Improved Sampling at the Subspecies Level Solves a Taxonomic Dilemma Â
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Molecular Phylogenetics and Evolution 107 (2017) 538–550 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Improved sampling at the subspecies level solves a taxonomic dilemma – A case study of two enigmatic Chinese tit species (Aves, Passeriformes, Paridae, Poecile) Christian Tritsch a, Jochen Martens b, Yue-Hua Sun c, Wieland Heim d,e, Patrick Strutzenberger a, ⇑ Martin Päckert a, a Senckenberg Naturhistorische Sammlungen, Königsbrücker Landstrabe 159, D-01109 Dresden, Germany b Institut für Zoologie, Johannes Gutenberg-Universität, 55099 Mainz, Germany c Key Laboratory of Animal Ecology and Conservation, Institute of Zoology, Chinese Academy of Science, 100101 Beijing, China d Institut für Biochemie und Biologie, AG Tierökologie, Universität Potsdam, Maulbeerallee 1, 14469 Potsdam, Germany e Amur Bird Project, Roseggerstrabe 14, 14471 Potsdam, Germany article info abstract Article history: A recent full species-level phylogeny of tits, titmice and chickadees (Paridae) has placed the Chinese Received 1 July 2016 endemic black-bibbed tit (Poecile hypermelaenus) as the sister to the Palearctic willow tit (P. montanus). Revised 25 November 2016 Because this sister-group relationship is in striking disagreement with the traditional affiliation of P. Accepted 9 December 2016 hypermelaenus close to the marsh tit (P. palustris) we tested this phylogenetic hypothesis in a multi- Available online 11 December 2016 locus analysis with an extended taxon sampling including sixteen subspecies of willow tits and marsh tits. As a taxonomic reference we included type specimens in our analysis. The molecular genetic study Keywords: was complemented with an analysis of biometric data obtained from museum specimens. Our phyloge- Poecile hypermelaenus netic reconstructions, including a comparison of all GenBank data available for our target species, clearly Poecile weigoldicus Multi-locus phylogeny show that the genetic lineage previously identified as P. hypermelaenus actually refers to P. weigoldicus Phylogeography because sequences were identical to that of a syntype of this taxon. The close relationship of P. weigoldi- DNA barcoding cus and P. montanus – despite large genetic distances between the two taxa – is in accordance with cur- rent taxonomy and systematics. In disagreement with the previous phylogenetic hypothesis but in accordance with most taxonomic authorities, all our P. hypermelaenus specimens fell in the sister clade of all western and eastern Palearctic P. palustris. Though shared haplotypes among the Chinese popula- tions of the two latter species might indicate mitochondrial introgression in this part of the breeding range, further research is needed here due to the limitations of our own sampling. Ó 2016 Elsevier Inc. All rights reserved. 1. Introduction pleteness of taxon sampling and the choice of target taxa at the species level also largely depend on the species concept applied Density of taxon sampling has been repeatedly evaluated as one and the taxonomic authorities consulted. Taking these basic con- of the crucial factors affecting the accuracy of phylogenetic analy- cerns into consideration, our study refers to a problematic sister- ses and the resulting topologies (Omland et al., 1999; Johnson, group relationship in a near-complete multi-locus phylogeny of 2001; Braun and Kimball, 2002; Zwickl and Hillis, 2002; Funk tits, Paridae (Johansson et al., 2013). and Omland, 2003; Heath et al., 2008; Albert et al., 2009; McKay Tits, titmice and chickadees of the speciose passerine family and Zink, 2010; Päckert et al., 2010; Nabhan and Sarkar, 2011). Paridae are widely distributed across Eurasia, Africa and North Adding missing taxa to an incomplete sampling might already America. Two diversity hotspots are situated in the western improve phylogenetic accuracy even with 50–90% missing Palearctic and along the eastern margin of the Qinghai-Tibet Pla- sequence information (e.g. only one out of n loci analyzed was teau (Fig. 1). Ancestral range reconstructions by Tietze and available for single taxa; Wiens and Tiu, 2012). However, com- Bothakur (2012) identified China as a cradle of diversity from where ancestors of Eurasian Paridae repeatedly colonized adjacent regions, such as the northern Palearctic, the Himalayas, Indonesia ⇑ Corresponding author. and the Philippines. High levels of species richness in the Heng- E-mail address: [email protected] (M. Päckert). duan Shan and the adjacent northern Chinese mountain systems http://dx.doi.org/10.1016/j.ympev.2016.12.014 1055-7903/Ó 2016 Elsevier Inc. All rights reserved. C. Tritsch et al. / Molecular Phylogenetics and Evolution 107 (2017) 538–550 539 Fig. 1. Worldwide distribution of tits, titmice and chickadees (Paridae); colours indicate local species richness from 1 (dark blue) to 11 (red) species; shapefiles downloaded from BirdLife International (2016). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) have been documented for several bird families and the complex cluster with all Chinese subspecies of the marsh tit (P. palustris) topography and landscape mosaic is regarded as the most impor- with this entire clade being the sister group of all willow tit (P. tant factor that made this region a center of avian endemism (Lei montanus) specimens (Fig. 2B). However, a multilocus phylogeny et al., 2006, 2014). This is reflected by pronounced intraspecific for all Paridae based on a near-complete sampling at the species phylogeographic structure in many bird species from China and level by Johansson et al. (2013) did not confirm this classification the adjacent eastern Himalayas (in Paridae, Parus minor: Zhao but recovered P. hypermelaenus as sister to the willow tit (P. mon- et al., 2012; Periparus ater: Martens et al., 2006; Tietze et al., tanus) with strong support (Fig. 2A). Apparently, the conflict 2011; Pentzold et al., 2013; in Aegithalidae, Aegithalos concinnus: between these two phylogenetic studies has remained unrecog- Dai et al., 2011). nized so far and cannot be resolved easily, because Dai et al. The first comprehensive phylogenetic family tree of Paridae was (2010) did not include western Palearctic marsh tit populations, exclusively based on the mitochondrial cytochrome-b gene (Gill whereas Johansson et al. (2013) did not include eastern Palearctic et al., 2005). As a consequence of this study several taxonomic marsh tit populations in their sampling. Clarification can only be authorities followed the lead of the American Ornithologists’ Union achieved with an improved taxon sampling including the Sichuan (AOU) who had already elevated the Nearctic Poecile and Baeolo- tit (P. weigoldicus) as a key taxon which was missing from most phus to genus rank (AOU, 1998) and divided the former Parus sensu previous phylogenetic studies (except Salzburger et al., 2002). lato into up to seven genera (former subgenera; see Gosler and This species is endemic to the south-western Chinese provinces Clement, 2007). Eight years later Johansson et al. (2013) published Sichuan, NW Yunnan, SE Qinghai and eastern Tibet (Harrap and the first near-complete multilocus species-level phylogeny includ- Quinn, 1996), where its breeding distribution widely overlaps with ing 56 parid species recognized by Gosler and Clement (2007) plus the scattered range of the black-bibbed tit, P. hypermelaenus. thirteen selected subspecies that raised their sampling to 69 parid Johansson et al. (2013) tentatively included P. weigoldicus in the taxa (covering all 67 Paridae species distinguished by Clements willow tit, P. montanus, following earlier classifications (Snow, et al., 2015 except one, see below). Apart from a confirmation of 1967; Quaisser and Eck, 2002; Gosler and Clement, 2007). Based the generic subdivision of Paridae, the new multi-locus phylogeny on its rather high genetic divergence from other P. montanus sub- included one rather surprising grouping in the Old World clade of species (4.6–5.9% K2P distance for cytochrome-b) documented by genus Poecile concerning the position of the black-bibbed tit (Poe- Salzburger et al. (2002) some authors had separated P. weigoldicus cile hypermelaenus). This species is a Chinese endemic with a from the willow tit at the species level before (see Table 1). Other restricted and presumably scattered distribution range in south- authors united all brownish-headed Asian willow tits and allies western China (Provinces Shaanxi, Sichuan, Yunnan, Guizhou – under the species name P. songarus (the ‘‘songar tit” including Cen- and probably also outliers to Hubei, Gansu and south-eastern tral Asian P. s. songarus and Chinese P. s. affinis, P. s. stoetzneri and P. Tibet) and isolated populations in the Chin Hills (south-western s. weigoldicus; see Table 1), but so far this arrangement has not Myanmar; Harrap and Quinn, 1996). been corroborated by molecular phylogenetics (Kvist et al., 2001; Classifications based on comparative morphology and biomet- Salzburger et al., 2002). A recent phylogeographic study by Song rics assigned P. hypermelaenus to close kinship of P. palustris et al. (2016) compared Chinese marsh tit and willow tit popula- (Vaurie, 1957; Harrap and Quinn, 1996; Eck, 2006) and most taxo- tions only without considering their trans-Palearctic counterparts nomic authorities agreed on this relationship (compare Table 1). and thus did not provide a finite solution of the systematic- This taxonomic