J Ornithol (2015) 156 (Suppl 1):S355–S365 DOI 10.1007/s10336-015-1185-6

REVIEW

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

1 2 3 4 Martin Pa¨ckert • Jochen Martens • Yue-Hua Sun • Dieter Thomas Tietze

Received: 31 October 2014 / Revised: 27 January 2015 / Accepted: 23 February 2015 / Published online: 12 March 2015 Ó Dt. Ornithologen-Gesellschaft e.V. 2015

Abstract As one of the most prominent topographical plateau several times independently. Second, we features on Earth, the Qinghai–Tibetan plateau (QTP) un- discuss younger speciation events corresponding to phy- derwent a long and complex history of the QTP uplift from logeographic east–west divides along the southern QTP the collision of the Indian and the Eurasian plates to the margin. A multidisciplinary approach combining genetic, present. At its southern and southeastern margins, it is bioacoustic and morphological markers shed new light on flanked by the most significant hotspots of organismic di- the phylogenetic relationships of Pnoepyga wren babblers versity of the northern hemisphere (including birds), the and on the intraspecific subdivision of the Buff-barred Sino-Himalayan mountain forests. In contrast, the central Warbler (Phylloscopus pulcher). plateau region itself harbours -poor communities but also a good number of endemics that presumably Keywords Qinghai–Tibetan plateau Á Passeriformes Á evolved from rather ancient (pre-Pleistocene) phylogenetic Sino-Himalayas Á Alpine habitats Á Carpodacus lineage splits. We discuss the evolutionary history of QTP from a twofold perspective including examples from our own research. First, we provide an overview of Introduction those alpine QTP endemics that represent late Miocene and Pliocene lineage splits, i.e. early colonisations to the cen- The Qinghai–Tibetan plateau (QTP) is one of the most tral alpine QTP region. As an example, true rosefinches prominent topographical features on Earth. The long and ( Carpodacus) presumably evolved from a forested complex history of the QTP uplift from the collision of the eastern QTP centre of origin and colonised the (semi-)open Indian and the Eurasian plates to the present has been much debated but is still not fully understood to date (reviews: Mulch and Chamberlain 2006; Favre et al. 2014). How- Communicated by E. Matthysen. ever, there is a growing understanding that the discussion of biogeographic history and organismic evolution (faunal & Martin Pa¨ckert [email protected] turnovers, colonisation events, continental radiations) of the QTP region cannot be limited to the central plateau 1 Senckenberg Natural History Collections, Museum of region alone, but is firmly associated with the orogenetic Zoology, Ko¨nigsbru¨cker Landstraße 159, 01109 Dresden, history of the flanking mountain chains: Tian Shan in the Germany 2 west, Himalayas in the south, Hengduan Shan in the Institut fu¨r Zoologie, Johannes Gutenberg-Universita¨t, southeast and Altai and Qilian Shan in the north (review in 55099 Mainz, Germany 3 Favre et al. 2014). At its southern and southeastern fringes, Key Laboratory of Ecology and Conservation, the QTP is flanked by the most significant hotspots of or- Institute of Zoology, Chinese Academy of Science, Beijing 100101, China ganismic and also avian diversity of the northern hemi- sphere, namely the Sino-Himalayan mountain forests 4 Institute of Pharmacy and Molecular Biotechnology, Heidelberg University, Im Neuenheimer Feld 364, (Myers et al. 2000; Wikramanayake et al. 2001; Roselaar 69120 Heidelberg, Germany et al. 2007). The remarkably high species richness of these 123 S356 J Ornithol (2015) 156 (Suppl 1):S355–S365 mountain forests strongly contrasts with low species di- recolonisation of the core plateau region from versity on the central QTP itself. However, some of the (north-)eastern glacial refugia (Qu et al. 2010; Lei et al. cold-adapted high alpine endemics of the plateau itself 2014). But going back in time and evolutionary history, have apparently evolved from rather ancient lineage splits diversification and speciation processes among eight and underwent long-term adaptation to extreme conditions species of snowfinches and among four Holarctic lin- (Qu et al. 2013). In fact, there is evidence from the fossil eages of the Horned were suggested to date back to record and from reconstructed biogeographic histories that even late Pliocene times (in fact with quite similar split the core QTP region was an evolutionary centre of origin ages estimates; Table 1;compareLeietal.2014; (Deng et al. 2011; Tseng et al. 2013; Wang et al. 2014)— Alstro¨metal.2013a). Possible evolutionary scenarios emphatically termed a ‘cradle of evolution’ of cold-adapted and taxonomic consequences are still under lively debate and forest-dwelling ground (Erithra and particularly for Horned because of a low signal of Pterostichus; Schmidt et al. 2012). nuclear markers and fundamental differences among In contrast, the discussion on the evolutionary history, split age estimates inferred from independent studies times and areas of origin of Tibetan endemic species (Alstro¨metal.2013a; Drovetski et al. 2014). To date, a has long been limited to young speciation processes centre of origin and diversification has not been hypo- during the final QTP uplift phase, in the course of thesised for either of these two groups, but at least for Quarternary climate change and glacial impact. But be- snowfinches a QTP ‘cradle of evolution’ is a quite likely cause comparative phylogeography is dealing with past hypothetical scenario that can be put to test in future demographic processes within species on a rather short studies (see below). evolutionary time scale—and in the case of previously With this paper, we aim at first providing a perspective studied QTP species only on a rather narrow spatial to the older pre-Pleistocene events and early lineage splits scale, too—this method only allows for reconstruc- within passerine genera and early colonisation events to the tions of the terminal events of colonisations and radia- central QTP from its fringes or from adjacent zoogeo- tions during the biogeographic history of a group of graphic regions. Second, we discuss the younger speciation organisms (Qu et al. 2009, 2010). For example, con- events with a focus on the frequently observed phylogeo- gruent phylogeographic scenarios for snowfinch species graphic east–west divides along the southern QTP margin of genera , Onychostruthus and Pyrgilau- under a multidisciplinary perspective from integrative da (Passeridae) as well as for the Horned Lark (Ere- . For both topics, we present some exemplary mophila alpestris, Alaudidae) suggested a post-glacial results from our own research.

Table 1 Split age estimates for Family Species/lineage Age References alpine QTP endemic species and species groups (genetic Paridae Pseudopodoces humilisa 7.7–9.9 Qu et al. (2013) lineages; split age from closest Fringillidae Carpodacus roborowskiia *9.0 Tietze et al. (2013) relative in Ma) Fringillidae Carpodacus pulcherrimus/C. waltoni cladea *7.0 Tietze et al. (2013) (genus) *9.0 Pa¨ckert et al. (2010, 2013) Aegithalidae Leptopoecile sophiae *4.0 Pa¨ckert et al. (2010, 2013) Phylloscopidae Phylloscpus fuscatus/P. fuligiventer clade *7.5 Pa¨ckert et al. (2012) Phylloscopidae Phylloscopus affinis/P. occisinensisa *4.0 Pa¨ckert et al. (2012) Turdidae Turdus mupinus *4.5 Nylander et al. (2008) Turdidae Turdus kessleria *1.0 Nylander et al. (2008) Muscicapidae Phoenicurus ochruros QTP clade 4.08 Qu et al. (2010) Passeridae Montifringilla/Pyrgilauda cladeb 3.8 Lei et al. (2014) Alaudidae Melanocorypha genus *6.5 Alstro¨m et al. (2013a) Alaudidae Melanocorypha maximaa *3 Alstro¨m et al. (2013a) Alaudidae gulgula *5 Alstro¨m et al. (2013a) Alaudidae Eremophila genus *9 Alstro¨m et al. (2013a) Alaudidae Eremophila alpestris (basal split) *3.5 Alstro¨m et al. (2013a) Alaudidae Eremophila alpestris QTP clade *2.5 Alstro¨m et al. (2013a) a Alpine endemic species according to Vaurie (1972) p. 139 b Except M. nivalis, all species of this clade are endemic to the QTP

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Fig. 1 Major periods of faunal interchange between mountain forests of the southern/southeastern QTP margins and adjacent bioregions, colour codes of key forest areas for SE Asian birds, according to Collar et al. (2001); modified from Pa¨ckert et al. (2012) (color figure online)

Forests of the southern QTP margins: hotspot relevant trigger of accelerated avian diversification at the of biodiversity southern and southeastern QTP margins during the mid- to late Miocene and first colonisation events to the subtropical Four major biodiversity hotspots at the western, southern forests of the Himalayas and the Hengduan Shan from a and eastern QTP margins have been listed by Favre et al. Southeast Asian/Indoburmese centre of origin were sug- (2014: fig. 1), all of them encompassing mountain forest gested to have occurred during that period (Pa¨ckert et al. ecosystems of (1) Central Asia, (2) the Himalayas, (3) 2012; Fig. 1). This early stage of passerine diversification Indo-Burma and (4) the Hengduan Shan. Species richness in SE Asia is backed by the recent finding that the mean patterns of Palearctic passerine birds almost perfectly re- split age of sister species pairs of the Eastern Himalayas flect these four centres (Roselaar et al. 2007; see review on was estimated as ancient as 7.1 Ma (Price et al. 2014)—the passerine diversity of the Sino-Himalayas in Martens et al. time when earliest lineage splits among subtropical sister 2011). In the south, where Sino-Himalayan mountain for- species are thought to have occurred (see the example of ests constitute the greatest biodiversity hotspot of the re- treecreepers, Certhia, in Fig. 2). Recent ecological com- gion, avian species richness increases along a gradient from munity analyses of Himalayan passerines have shed some the drier Western Himalayas towards highest species light on adaptive processes and niche evolution. Differ- richness in the southeast (Price et al. 2003, 2011; 358 ences among species in body size and shape as well as in species of Passeriformes alone were counted in the south- foraging and feeding strategies had apparently already eastern Indian Himalayas in the most recent study by Price evolved in the early stages of SE Asian passerine radiations et al. 2014). The same differences of biodiversity indices long before ancestors of extant species occupied their among regions were found when comparing species rich- elevational niches in the respective Sino-Himalayan ness hotspots of the Qilian and Hengduan mountains with vegetation belts (Price 2010; Kennedy et al. 2012; Price those of the Western Himalayas and Central Asian moun- et al. 2014). tains and the northern Chinese plains (Lei et al. 2006; data for threatened birds only!). Furthermore, a similar longi- tudinal species richness gradient was recently confirmed Out of Tibet: the QTP a cradle of evolution? for vascular plants having a higher diversity in the eastern QTP region (Yang et al. 2013). Forest biodiversity hotspots of the QTP margin sharply The onset and intensification of the Southeast Asian contrast the central plateau region which is characterised monsoon system during that time was suggested as one by a rather cold and dry climate—with local annual mean

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Fig. 2 Ecological segregation and parapatry along elevational gradi- elements and only one (C. hodgsoni; with C. h. mandellii in the ents in the Himalayas, the treecreepers (Certhia; drawings, K. Himalayas, drawing) represents a Palearctic faunal element from a Rehbinder) of Central Nepal (forest vegetation profile modified from Pleistocene faunal interchange among the Palearctic and the mountain Martens and Eck 1995; longitude of the upper Kali Gandaki Valley). forests of the southern/southeastern QTP margins (phylogeny Four species occupy different forest belts with partly overlapping modified from Tietze et al. 2006 and Pa¨ckert et al. 2012) elevational niches: three species represent (sub)tropical Asian faunal precipitation as low as 100–300 mm—and low species harbours a good number of greatly distinctive endemics in richness of and plants (Favre et al. 2014). Indices all animal groups hitherto studied. In his comprehensive of ‘‘bird richness’’ by Wikramanayake et al. (2001) differ review of the avifauna of Tibet, Vaurie (1972) provided a greatly between forest ecoregions and those of the alpine first list of 13 endemic species (6 of them considered strict habitats: indices for Himalayan broadleaf and subalpine endemics) from the high-elevation habitats of the central conifers vary between 202 and a maximum diversity of 490 QTP region. He further added an extended list including a in the Eastern Himalayas, while alpine steppes and mead- number of ‘‘species which are distinctive of Tibet’’ but ows of the dry Plateau region habour a considerably lower whose ranges extend towards or even beyond the margins diversity (indices of 115 and 171; Wikramanayake et al. of the plateau to High Central Asia, the Sino-Himalayas 2001). Regional endemism is also higher in the Himalayan and the Old World Eremian deserts of Mongolia, Turkestan forests when referring to single ecoregions (indices of 9–11 and the Middle East (Vaurie 1972). Later, Weigold (2005, in Himalayan broadleaf forests vs. 0–1 in the alpine pp. 114–117) listed many of them as ‘‘first degree en- ecoregions). Nevertheless, the central QTP region also demics’’ and character species for different subregions of

123 J Ornithol (2015) 156 (Suppl 1):S355–S365 S359 the plateau, e.g. Carpodacus roborowskii for the eastern are a good number of ‘‘high plateau endemics’’ (Lei et al. border of Changtang cold steppe or the Tibetan , 2014) that evidently date back to more ancient colonisation Emberiza koslowi, as an ancient autochthonous endemic of events long before the onset of the Pleistocene. Meanwhile, the treeless grasslands. Weigold (2005) was indeed among several phylogenetic studies have provided rough split-age the first who suggested Tibet as an autochthonous centre of estimates for at least a number of alpine QTP endemics organismic evolution. The Weigoldian Tibetan origin hy- (Table 1). Results from molecular dating studies confirm pothesis received recent support from phylogeographies of the hypothesis that the oldest ancestors of some QTP forest-dwelling ground beetles of the Himalayas (Schmidt species (namely some of the classical endemics listed by et al. 2012) and recently became famous as the ‘‘Out of Vaurie 1972) had already first settled the plateau region in Tibet’’ hypothesis based on fossil evidence from the Plio- the mid- to late Miocene between 9 and 7 Mya ago—the cene cold-adapted fauna of the Zanda Basin of same period when early diversification of SE Asian forest southwestern Tibet (Deng et al. 2011; Tseng et al. 2013; passerines took place (Table 1). After successful coloni- Wang et al. 2014). So the high elevations of Tibet in- sation of plateau habitats, ancestors of extant endemic cluding the QTP margins might also turn out as a cradle of species underwent significant morphological adaptations to origin for some groups of the extant passerine fauna (Tietze the open alpine habitats that obscured their phylogenetic et al. 2013; Lei et al. 2014). In fact, there is firm evidence affinities in such a way that traditional systematics had that, during that period of the QTP uplift, vast parts of the misplaced a few of them even into the wrong taxonomic plateau region had already reached altitudes comparable to family. The Tibetan Ground (Pseudopodoces humilis, those of today (Mulch and Chamberlain 2006; Favre et al. Paridae) had been wrongly placed in the (James 2014: fig. 3) and that ecological niches for forest and alpine et al. 2003; Johansson et al. 2013). The Tibetan Rosefinch bird communities existed even on the plateau itself. Ac- Carpodacus roborowskii had long been in a monotypic cording to Wu et al. (2007), from the early Miocene on, genus of its own (Kozlowia) and considered a close relative large areas on the QTP were covered by vast lakes sur- of the alpine and arctic Leucosticte mountain finches or of rounded by conifer forests that, during progressive cooling Montifringilla snowfinches (Clement 1999); however, this and drying after the desiccation of large lakes, persisted species was recently shown to be firmly nested in the ‘‘true and dominated the plateau forest assemblages but were rosefinches’’ of genus Carpodacus (Zuccon et al. 2012; partly replaced by mixed forests including oak and walnut Tietze et al. 2013; Fig. 3). Tit-warblers of genus Lep- species. topoecile had long been placed either in the or the Regulidae but meanwhile were shown to be an ancient branch of the Aegithalidae (Pa¨ckert et al. 2010). And, fi- Early colonisations of the central QTP alpine nally, the enigmatic Przewalski’s Urocynchramus plateau habitats pylzowi had been placed in close affinity to the buntings (Emberizidae) by some authors and to the finches (Frin- While spatial and timely scenarios of evolutionary history gillidae) by others, but meanwhile this species was also are quite elaborate for many groups of QTP forest pas- suggested to be a rather ancient and isolate taxon without serines, the alpine endemics of the plateau region itself any close relatives (Groth 2000; Yang et al. 2006). have so far been largely studied with a focus on their Recently, more insight into adaptation to high-elevation Quarternary demographic history (Qu and Lei 2009;Qu habitats of QTP endemics resulted from a comparative et al. 2009, 2010; Yang et al. 2009; Lei et al. 2014). Along genomic study: for the Tibetan Ground Tit (Pseudopodoces with these, the discussion on avian speciation timing on the humilis), Qu et al. (2013) demonstrated positive selection QTP (and/or along its margins) has been much limited to on genes linked with energy metabolism and skeletal de- the three late stages of QTP uplift (i.e. starting with the velopment both associated with adaptations to a ground- Qingzang movement 3.6 Mya ago to the end of the Gonghe dwelling life and extreme environmental conditions at high movement 150 kya ago; review in Lei et al. 2014). How- elevations. What has remained enigmatic so far is whether ever, there is a growing awareness of faunal turnovers these endemic QTP species never diversified to a notable during more ancient stages during the QTP uplift (review degree during long-term isolate evolution or whether they in Favre et al. 2014) as well as of more ancient speciation represent relic lineages of a formerly more diverse clade. In processes considerably predating the Pleistocene era that the latter case, extinction is to be considered as a relevant mainly formed the avian communities of subtropical for- process that shaped avian communities on the QTP. In fact, ests at the southern QTP margin (Song et al. 2009;Pa¨ckert a possible role of extinction events during avian radiations et al. 2012; Lei et al. 2014; Price et al. 2014). is quite likely and cannot be excluded, but must remain Apart from a glacial impact on intraspecific diversifi- subject to further studies. On the other hand, a few ancient cation and speciation processes on the plateau itself, there alpine lineages have diversified into several extant QTP 123 S360 J Ornithol (2015) 156 (Suppl 1):S355–S365

Fig. 3 Evolutionary history of true rosefinches (Carpodacus; modified from Tietze et al. 2013; phylogeny based on 3212 bp of concatenated cytb, ND2, myo, GAPDH; three taxa previously assigned to different genera: Kozlowia roborowskii, Haematospiza sipahi and Chaunoproctus ferreorostris). Ancestral state analysis of breeding habitats (Mesquite, maximum parsimony, characters unordered; traced over 21,000 trees from MrBayes analysis; branch lengths indicated according to the scale at the right); ancestral ranges inferred from maximum likelihood reconstructions with Lagrange (Tietze et al. 2013) indicated for selected nodes ([4 = more than four regions were inferred as ancestral range; biogeographic regions A–I indicated on map; numbers behind letters indicate the number of species occurring in one region); two clades of alpine species with partly different preferences highlighted by grey boxes (I, II)

species that even occur in wide-range sympatry on the Carpodacus (Tietze et al. 2013). The hotspot of extant plateau itself. Possibly the best studied alpine QTP en- species richness was inferred as the geographic origin of demics so far are the snowfinches of genera Montifringilla, the entire genus and, strikingly, breeding species of semi- Pyrgilauda and Onychostruthus: six endemic QTP species open and open plateau habitats were nested in the same diversified as late as 3.5 Mya (Qu et al. 2006; Lei et al. clades with true forest species throughout the entire Car- 2014) and only one of them dispersed far beyond the podacus phylogeny. For further illustration, we coded realms of the QTP to the Western Palearctic, i.e. the White- habitat preferences into six categories according to the winged Snowfinch, Montifringilla nivalis. In that respect, information given in del Hoyo et al. (2010), mapped them the snowfinches are one prominent example of Pleistocene on the original multilocus phylogeny of Tietze et al. (2013) in situ speciation on the central plateau region itself. and performed an ancestral-state analysis with Mesquite 2.5 (Maddison and Maddison 2008; Fig. 3; maximum parsimony, unordered characters, traced over 21,000 trees True rosefinches (Carpodacus): a Palearctic in to account for phylogenetic uncertainty). Ac- radiation from the QTP fringes cording to the results of ancestral range and ancestral habitat analyses, Carpodacus rosefinches evolved from a While times of origin have been estimated for quite a forested centre of origin at the southeastern QTP margin number of alpine passerine clades and species (Table 1), and colonised the alpine habitats of the central plateau the geographic origin of many QTP endemics is still ob- several times independently (Fig. 3). Strikingly, some of scure. For example, the area of origin was ambiguous for the alpine clades differed with respect to (ancestral) habitat the Tibetan Ground Tit, P. humilis, in an ancestral range preference: three species represent a typical open-habitat analysis by Tietze and Borthakur (2012). Recent evidence clade (with a strong preference of rocky hill slopes; Fig. 3, of multiple independent colonisations of the QTP centre clade I, including C. roborowskii as one alpine endemic) from its margins came from true rosefinches of genus while another alpine clade comprises species having

123 J Ornithol (2015) 156 (Suppl 1):S355–S365 S361 stronger affinities to semi-open alpine shrub and meadows (except allopatric speciation leading to extant vicariance) (Fig. 3, clade II). However, where species of these two on the plateau itself including possible short-term eco- clades locally co-exist in the same habitat they occupy logical segregation among alpine habitats (semi-open shrub different niches with respect to the size and variation of vs. alpine meadows vs. rock; see Fig. 3). food items (smaller vs. bigger grains) and height of nesting sites (C. rubicilloides and C. waltoni eos in the Xiongse Valley near Lhasa; Lu et al. 2011). Like snowfinches, even More tip branches growing: insight the alpine sister species of rosefinches of these two clades from phylogeography and integrative taxonomy (Fig. 3, I and II) occur in almost full-range sympatry. Possible differences in breeding habitat preferences of Recent intraspecific diversification and interspecific dif- sister species C. pulcherrimus and C. waltoni throughout ferentiation processes, e.g. due to Pleistocene range frag- their sympatric range have been preliminarily evaluated mentation and Holocene range expansion, have resulted in (del Hoyo et al. 2010; Tietze et al. 2013), but these are one very common phylogeographic pattern: east–west di- based on very scarce field data that have not yet been fully vides along the southern margin of the QTP. Most splits confirmed for the newly split species of this group, so involve one Himalayan species or genetic lineage versus a support from further field studies is needed here. second (and even a third one) from the Indo-Burmese According to these few case studies, the wide-range mountains and/or the Hengduan mountains and adjacent sympatry observed from some alpine sister species of the regions, respectively. Typically, E–W divides are observed central QTP strongly contrasts the phylogeographic pattern in (or among) high-elevation (sister) species and corre- of Pleistocene vicariance found in many forest-dwelling spond to vicariance due to Pleistocene range fragmentation passerines at the QTP margins (Pa¨ckert et al. 2012; and (Martens et al. 2011;Pa¨ckert et al. 2012). Whether the below). That might hint to a different mode of speciation extant representatives of such comparatively young genetic

Fig. 4 Evolutionary history of Asian Wren-Babblers (Pnoepygidae; (Himalayas, Indo-Burmese mountains, SW China), the Sino-Hi- modified from Pa¨ckert et al. (2013), phylogeny based on 3457 bp malayan high-elevation species (Pnoepyga albiventer) shows in- concatenated cytb, ND2, GAPDH, TGFB and ODC); genetic traspecific differentiation among three separate clades and indicates distances (cytochrome b) indicated between clades; two species pairs species status; genetic differentiation is strongly backed by differ- occur in elevational parapatry along the southern QTP margin ences in song (sonagrams at the right) 123 S362 J Ornithol (2015) 156 (Suppl 1):S355–S365

Fig. 5 Intraspecific differentiation of the Buff-barred Warbler (Phyl- two clusters separated by six substitutions (subspecies analysed loscopus pulcher; photo, J. Ferdinand) modified from Pa¨ckert et al. indicated according to cluster colour); sonagrams of songs shown (2014); sampling localities shown on map (circles sequenced below, verse structure indicated by uppercase letters above single samples, triangles song recordings, w two wintering records); the notes haplotype network (based on 817 bp cytochrome b) is divided into lineages have undergone effective shifts in morphological parapatry (Fig. 4). An E–W divide was expectedly found in or behavioural traits—that are biologically meaningful in the high-elevation species (P. albiventer) with even three the sense of species recognition and/or reproductive bar- lineages involved (however, C Himalayan populations of riers—can be put to test in a multidisciplinary approach P. pusilla remain to be studied). All four species can be including morphological, ecological and behavioural ana- well distinguished by their songs, and even intraspecific lyses, recently termed ‘‘integrative taxonomy’’ (Padial genetic differentiation of P. albiventer corresponds to song et al. 2010; Schlick-Steiner et al. 2010). In case of be- divergence across the E–W divide (Fig. 4). Whether havioural traits, passerine species having a rather stereo- structural differences between songs of lowland species typed territorial song with low intra- and interindividual (simple whistles) and high-elevation species (more com- variation provide optimal model groups, particularly spe- plex and variable songs) are adaptive to different forest cies-poor genera such as kinglets and treecreepers (Pa¨ckert environments is not fully explored but might be related to et al. 2003, 2009; Tietze et al. 2008). Two examples from choice of song perch and habitat preference (Pa¨ckert et al. our own team might illustrate this approach. 2013). High-pitched songs of P. immaculata might have Wren-babblers of genus Pnoepyga represent a rather evolved in adaptation to noisy habitats along mountain ancient lineage and a family of their own (Pnoepygidae; streams as suggested for some other passerines of the Hi- Gelang et al. 2009) that already started to diversify into malayan torrent-accompanying guild such as Phylloscopus four extant species in the late Miocene about 14 Mya ago magnirostris (Martens and Geduldig 1990). (Pa¨ckert et al. 2012). Their extant Sino-Himalayan distri- Cases of cryptic diversity within species—such as ex- bution is typically that of two species pairs in elevational emplified for Pnoepyga albiventer above—have become 123 J Ornithol (2015) 156 (Suppl 1):S355–S365 S363 more frequently observed along with the increasing num- received research grants from the National Natural Science Founda- ber of phylogeographic studies. In the course of these, tion of China, project No. 31272286. D.T.T. was funded by the Deutsche Forschungsgemeinschaft (Ti 679/1-1, Ti 679/2-1) and re- more genetic units within species have been discovered ceived travel grants for the IOC in Tokyo by the German Academic that correspond to further cases of phylogeographic divides Exchange Service (DAAD). We would like to thank all colleagues along the QTP margins, particularly in the species-rich who contributed to this symposium and to those who participated in regions of its southeast (Song et al. 2009; Dai et al. 2011; the successive fruitful discussions—you all made this meeting a big success. Zhao et al. 2012). Yet, cryptic diversity is still being de- tected in speciose families like leaf warblers (Phyllo- scopidae), e.g. by Alstro¨m et al. (2010). This family References comprises many Asian representatives distributed along the QTP margins, and local parapatry across elevational gra- Alstro¨m P, Davidson P, Duckworth JW, Eames JC, Le TT, Nguyen C, Olsson U, Robson C, Timmins R (2010) Description of a new dients can involve 8–11 species in the Himalayas and also a species of Phylloscopus warbler from Vietnam and Laos. Ibis maximum of 11 sympatric species on Taibai Shan of 152:145–168 Qinling mountains in China (Martens 2010: fig. 1; Price Alstro¨m P, Barnes KN, Olsson U, Barker FK, Bloomer P, Khan AA, 2010; Alstro¨m et al. 2013b). To date, only three Asian Qureshi MA, Guillaumet A, Crochet P-A, Ryan PG (2013a) Multilocus phylogeny of the avian family Alaudidae (larks) Phylloscopus species have been considered to have a more reveals complex morphological evolution, non-monophyletic or less continuous breeding distribution along the southern genera and hidden species diversity. Mol Phylogenet Evol QTP margin without any notable intraspecific phylogeo- 69:1043–1056 graphic structure, until this assumption was recently falsi- Alstro¨m P, Olsson U, Lei FM (2013b) A review of the recent advances in the systematics of the avian superfamily . fied for one of them, the Buff-barred Warbler, Chin Birds 4:99–131 Phylloscopus pulcher. This species was shown to be di- Clement P (1999) and sparrows. 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Auk 117:787–791 titude of nearly annual expeditions of J.M. to various parts of Asia James HF, Ericson PGP, Slikas B, Lei F, Gill FB, Olson SL (2003) from the year 1969 until today. We would like to thank the numerous Pseudopodoces humilis, a misclassified terrestrial tit (Paridae) of colleagues and helpers in various countries from whom we got in- the Tibetan plateau: evolutionary consequences of shifting valuable support in many respects. During the years, J.M. received adaptive zones. Ibis 145:185–202 several grants from Deutsche Ornithologen-Gesellschaft (DO-G), Johansson US, Ekman J, Bowie RCK, Halvarsson P, Ohlson JI, Price Gesellschaft fu¨r Tropenornithologie (GTO) and from Feldbausch- TD, Ericson PGP (2013) A complete multilocus species Stiftung and Wagner-Stiftung, both at Fachbereich Biologie, Johannes phylogeny of the tits and chickadees (Aves: Paridae). Mol Gutenberg-Universita¨t Mainz, Germany. Our current studies on QTP Phylogenet Evol 69:852–860 passerine evolution as well as travel funds for participation in the Kennedy JD, Weir JT, Hooper DM, Tietze DT, Martens J, Price TD Sino-Himalaya symposium at the IOC in Tokyo 2014 were granted (2012) Ecological limits on diversification of the Himalayan core by Deutsche Forschungsgemeinschaft, PA 1818/3-1 (MP). Y.-H.S. Corvoidea. Evolution 66:2599–2613

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