Jochen Martens

Niche filling slows the diversification of Himalayan songbirds

Speciation generally involves a three-step process—range expansion, range fragmentation and the development of reproductive isolation between spatially separated populations. Speciation relies on cycling through these three steps and each may limit the rate at which new species form. We estimate phylogenetic relationships among all Himalayan songbirds to ask whether the development of reproductive isolation and ecological competition, both factors that limit range expansions, set an ultimate limit on speciation. Based on a phylogeny for all 358 species distributed along the eastern elevational gradient, here we show that body size and shape differences evolved early in the radiation, with the elevational band occupied by a species evolving later. These results are consistent with competition for niche space limiting species accumulation. Even the elevation dimension seems to be approaching ecological saturation, because the closest relatives both inside the assemblage and elsewhere in the Himalayas are on average separated by more than five million years, which is longer than it generally takes for reproductive isolation to be completed; also, elevational distributions are well explained by resource availability, notably the abundance of arthropods, and not by differences in diversification rates in different elevational zones. Our results imply that speciation rate is ultimately set by niche filling (that is, ecological competition for resources), rather than by the rate of acquisition of reproductive isolation.

Genetic differentiation and phylogenetic relationships of Bonelli's Warbler Phylloscopus bonelli and Green Warbler P. nitidus

The mitochondrial genetic differentiation and molecular phylogenetic relationships of western and eastern Bonellis Warblers (Phylloscopus b. bonelli, P. b. orientalis) and Green Warbler Phylloscopus nitidus were investigated. The cytochrome b gene was amplified by polymerase chain reaction and 1038 nucleotides were sequenced directly in these and several other Phylloscopus species plus Sylvia atricapilla and Acrocephalus scirpaceus. The mitochondrial genetic distance between eastern and western Bonellis Warblers was as large (8.3-8.6%) as between each of them and the Wood Warbler P. sibilatrix. Compared to the amount of mtDNA differentiation between other closely related species and subspecies of birds, the divergence between the Bonellis warblers is far greater than among typical subspecies. Together with the distinct differences in calls and structure of song elements the genetic data support full species status of the two taxa. The cytochrome b sequence of P. nitidus differed by 2.5-3.1% from P. trochiloides, to which it is most closely related. This divergence is also larger than between most subspecies of birds studied so far at this locus and is consistent with the placement of P. nitidus as an allospecies within the superspecies P. [trochiloides]. We discuss population-genetic scenarios for a potentially accelerated rate of mtDNA differentiation in relatively small, geographically isolated populations that might help to explain the large sequence divergence observed. A phylogenetic tree was constructed by maximum parsimony and neighbour-joining. Chiffchaff P. collybita and Willow Warbler P. trochilus are sister species and together form the sister group of Bonellis and Wood Warblers. As expected, Arctic Warbler P. borealis was found to be the sister species of the Greenish Warbler complex (including nitidus), whereas the relationships of P. (inornatus) humei relative to the other species could not be resolved. Among the taxa studied, those without wing-bars belong to a phylogenetically older clade than those with wing-bars. MtDNA sequence data promise to be very useful in quantifying the genetic differentiation and phylogenetic relationships among closely related species, especially in morphologically poorly differentiated genera like Phylloscopus.

Evolution and genetic structure of the great tit (Parus major) complex

The great tit complex is divided into four groups, each containing several subspecies. Even though the groups are known to differ markedly on morphological, vocal and behavioural characters, some hybridization occurs in the regions where they meet. The great tit has often been referred to as an example of a ring species, although this has later been questioned. Here, we have studied the genetic structure and phylogenetic relationships of the subspecies groups to clarify the evolutionary history of the complex using control region sequences of the mitochondrial DNA. The subspecies groups were found to be monophyletic and clearly distinct in mitochondrial haplotypes, and therefore must have had long-independent evolutionary histories. This conflicts with the ring species assignment and supports the formation of secondary contact zones of previously temporarily isolated groups. According to the phylogenetic species concept, all the subspecies groups could be considered as separate species, but if the definition of the biological species concept is followed, none of the subspecies groups is a true species because hybridization still occurs.

A case of possible vocal convergence between frogs and a bird in Himalayan torrents

Several species of frogs of the subgenusRana (Paa) and one species of bird of the genusPhylloscopus, which are calling in or near torrents in the Himalayas, show striking similarities in their vocal signals: 1) The calls are composed of short sequences of notes separated by periods of silence; 2) the notes are pure, short, and have a narrow frequency band; 3) within each sequence, the notes are rhythmically emitted. We suggest that these characteristics may be adaptive, the convergence being caused by the selective pressure of the acoustic constraints of the biotope. Mehrere Frosch-Arten der UntergattungRana (Paa) und ein Laubsänger der GattungPhylloscopus, die in oder in unmittelbarer Nähe von Gebirgsflüssen des Himalayas leben, weisen in ihren akustischen Signalen bemerkenswerte Ähnlichkeiten auf. 1) Die Rufe bzw. Gesänge setzen sich aus kurzen Folgen von Elementen zusammen, die durch lange Pausen getrennt sind. 2) Die Elemente sind rein und kurz; ihre Frequenzbänder sind schmal. 3) Innerhalb jeder Ruffolge werden die einzelnen Elemente rhythmisch geäußert. Wir vermuten, daß diese Eigenschaften adaptiv sind. Derart ähnliche Rufe bei nur weitläufig verwandten Tiergruppen würden somit auf Konvergenz beruhen, hervorgerufen durch den Selektionsdruck der akustischen Eigenschaften des Biotops.

Paraphyly of the Blue Tit (Parus caeruleus) suggested from cytochrome b sequences

The phylogenetic relationships of the Blue Tit-Azure Tit assemblage (genus Parus; Aves: Passeriformes) were studied using mitochondrial DNA sequences of 24 specimens representing seven subspecies from Eurasia and North Africa. Previous work based on comparative morphological and acoustic data suggested a division of the Blue Tit (Parus caeruleus) into two species. Our analyses clearly indicate that the Blue Tit represents a paraphyletic assemblage, including a European/Middle Asian clade that is the sister group to the Azure Tit (Parus cyanus) and a North African clade. The North African clade (teneriffae subspecies group) is a sister group to the European Blue Tit/Azure Tit clade. We suggest a division of the Blue Tit into two separate species, Eurasian Blue Tit (Parus caeruleus s. str.) and African Blue Tit (Parus teneriffae). However, our data give no support for assigning species rank to Parus cyanus flavipectus, a subspecies of the Azure Tit, as suggested by several authors on morphological grounds.

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.

Phylogeography of a Palaearctic sedentary passerine, the willow tit (Parus montanus)

We analysed variation of the mitochondrial control region from willow tits through its Palaearctic distribution range. Although we found high amount of genetic variation (π=1.114%), there was almost no differentiation between subspecies or geographical localities. This may be because of a combination of several ecological and genetic factors, including a relatively homogenic habitat through the distribution range, lack of geographical barriers, high gene flow and a large long‐term effective population size. On the contrary, in the songar tit, which is sometimes considered to be conspecific with the willow tit, the mitochondrial lineages seem to correlate with the geographical locality and are clearly distinct from the willow tit. We concluded that the common ancestors of willow and songar tits existed some 1.5–2 Myr ago in the south‐eastern Asia. After the last Ice Ages, the willow tit expanded all through the Palaearctic, whereas the songar tit remained in eastern Asia.

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.

Radiation and species limits in the Asian Pallas’s warbler complex ( Phylloscopus proregulus s.l.)*

Pallas’s Warbler (Phylloscopus proregulus) of the Eastern Palaearctic (Siberia, China, Himalayas) resolves into a complex of four closely related but distinct allospecies forming a superspecies, P. [proregulus]. Assignment of species rank is based on cytochrome-b gene sequences and on vocalisations (territorial song and calls). Morphological divergence is poor, as is typical in Phylloscopus. It applies to size (nominate Siberian proregulus as opposed to the Sino-Himalayan taxa), and slight coloration differences among the latter taxa do not correspond to the cyt-b topology and are considered to be adaptive. Vocal differences relate to syntax (verse song vs endless song), frequency (broad vs narrow bandwidth, allocation of elements within the frequency band), form of elements (ascending vs descending parts, combination of these), and repertoire size. Strong premating isolating mechanisms are assigned to vocalisations. Contrary to current taxonomy, we propose the following constituent taxa of the Phylloscopus [proregulus] complex: Phylloscopus proregulus s.str. (Siberia, disjunct from the following taxa), P. kansuensis (China: Gansu, Qinghai), P. forresti (W/SW China, part of E Himalayas?), P. chloronotus with two subspecies: P. c. simlaensis (W Himalayas), and P. c. chloronotus (C and E Himalayas). Contact zones and possible hybridisation between the Sino-Himalayan taxa remain undetermined. A closely related isospecies is Phylloscopus yunnanensis (syn. P. sichuanensis), which is locally sympatric with and extremely similar morphologically to P. forresti and P. kansuensis. Cyt-b distance values range from 3.1% to 4.6% within the P. proregulus complex and from 7.5% to 8.4% between the latter and P. yunnanensis. This corresponds to differentiation times of 4.1 to 5.5 Myears (P. proregulus complex vs P. yunnanensis) and 1.7 to 3.2 Myears (within the P. proregulus complex).

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.