A molecular phylogeny of bullfinches Pyrrhula Brisson, 1760 (Aves: Fringillidae)

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Abstract

We present a molecular phylogeny of bullfinches (Pyrrhula Brisson, 1760) based on 2357 bp DNA sequence information of mitochondrial genes (cyt-b, 16S rRNA) and nuclear introns (fib-7, GAPDH-11). The genus is clearly a monophyletic group. Within the limits of Pyrrhula, molecular methods support the subdivision of three main groups: (1) “Southeast-Asian bullfinches” (P. nipalensis and P. leucogenis), (2) “Himalayan bullfinches” (P. aurantiaca, P. erythaca, P. erythrocephala), and (3) “Eurasian bullfinches” (P. pyrrhula s.l.). Within the last group there are four different subgroups: (3a) P. (p.) murina, (3b) P. (p.) cineracea, (3c) P. (p.) griseiventris, and (3d) P. pyrrhula s.str. The centre of origin of the genus Pyrrhula was most probably Southeast Asia. Incomplete lineage sorting of both mitochondrial and nuclear genes is observed among two apparently good species (P. erythaca and P. erythrocephala) indicating a very recent speciation event within the Himalayan Mountain chain. According to our estimates, the Pyrrhula ancestors split from the Pinicola ancestors before the Pleistocene. Apart from the subsequent Pre-Pleistocene splits of the three ancestral main groups, most of the diversification of today’s representatives probably took place during the past 600,000 years, possibly in interaction with Pleistocene refugia and successive colonization movements after the last glaciation. Thus our work confirms the traditional delimitation of the bullfinches towards the other members of the finch family Fringillidae and corroborates most of the classic intra-generic subdivisions.

Research highlights

► Pyrrhula is clearly a monophyletic group (subdivided into three main groups). ► Centre of origin of the genus Pyrrhula was most probably Southeast Asia. ► Radiation in interaction with Pleistocene refugia. ► Most of the diversification of today’s representatives happened during the past 600,000 years. ► Successive colonization movements took place after the last glaciation.

Introduction

Unlike other taxonomic groups of birds, the systematic position of the bullfinches of the genus Pyrrhula has not been particularly controversial. For a long time the integrity of the genus as a clearly defined phylogenetic unit was taken for granted, in part because of the fairly good accordance of morphological traits and geographic distribution patterns. Thus the genus Pyrrhula served as a prominent example for classic studies of patterns of ancestry and their geo-historic background (Bianchi, 1907; Voous, 1949). Most of the systematic discussion concerned intra-generic relationships, mainly in the P. pyrrhula group, that basically dealt with the validity of species rank of some taxa (Voous, 1949, Vaurie, 1956).

The bullfinches form a relatively well defined genus comprising only six currently recognized species (Dickinson, 2003, Clements, 2007). The Eurasian Bullfinch (P. pyrrhula) is its most widely distributed member with a breeding range covering the entire northern Palearctic region from the British Isles to the Far East. The males of the East Asian-Japanese subspecies griseiventris and the Siberian subspecies cineracea differ from the nominate and other western subspecies in lacking red underparts: griseiventris has red cheeks and a pinkish belly, cineracea has completely grey cheeks and underparts. They are sometimes treated as separate species by some authors (Stepanyan, 1991). Another morphologically distinct relative of the Eurasian bullfinches, the Azores Bullfinch P. (pyrrhula) murina is endemic to a single mountain slope of Pico da Vara on the Azorean main island São Miguel. Due to its remoteness and the small population estimates this taxon was consequently ranked “critically endangered” on the IUCN Red List (IUCN, 2010).

Four Southeast-Asian species are native to the Sino-Himalayan mountain ranges. The Red-headed Bullfinch P. erythrocephala inhabits the high-altitude coniferous and mixed birch and larch forests (2700–4200 m) of the Himalayas from Kashmir and northern Punjab through Nepal to Tibet, Sikkim and Eastern Buthan. It is geographically replaced by the Beavan’s Bullfinch, P. erythaca, in the Eastern Himalayas and SW Chinese provinces southward to Yunnan and over a large distributional gap also on Taiwan. Because males of both species have intense orange-red underparts and both sexes share a similar head pattern they were unanimously considered close relatives. Their distribution in the Himalayas is poorly known and no data exist on local sympatry or hybridisation (cf. Wunderlich, 1992a, Martens and Eck, 1995: 419–421, for breeding ranges in the Himalayas). The vicariant Orange Bullfinch, P. aurantiaca, is restricted to a small range in the western Himalayas and adjacent Kashmir and Punjab (Wunderlich, 1992b). The Brown Bullfinch P. nipalensis differs considerably from the latter three congeners in having a more uniform plumage in both sexes and unlike the high-altitude species prefers rather subtropical conditions at median altitudes (1350–3300 m) in the Himalayas and Chinese mountains and on Taiwan (Clement, 1993). Finally, the Philippine Bullfinch P. leucogenis is the only species of the genus inhabiting the Indomalayan Region with populations on Luzon (nominate leucogenis) and on Mindanao (ssp. steerei; Clement, 1993).

Molecular systematic methods allowed a moderate re-assessment of the integrity and structure of the genus Pyrrhula. The most extensive previous cytochrome-b study suggests monophyly of the genus (Arnaiz-Villena et al., 2001). However, it contains only five Pyrrhula taxa. P. nipalensis was named to be the sister clade to all other study species among which all P. pyrrhula subspecies formed a distinct sister clade to the P. erythaca branch. Owing to the close relationship of bullfinches and grosbeaks Pinicola, one of the more challenging suggestions from this study was the proposal to unify Pyrrhula and Pinicola in one genus (Arnaiz-Villena et al., 2001). Another point is the potential species rank of the Azores Bullfinch P. (pyrrhula) murina (Bibby et al., 1992, Aubrecht, 2000). However, there is no comprehensive molecular phylogenetic study of Pyrrhula to date that takes into account the taxonomic status of several subspecies. Thus the aim of this study was to identify molecular relationships based on mitochondrial and nuclear genes between all six currently accepted Pyrrhula species, including fifteen of 24 currently accepted taxa according to Dickinson (2003). Based on these data, we draw phylogenetic conclusions and offer hypotheses that could explain the intra-generic differentiation patterns of Pyrrhula.

Section snippets

Material and methods

Our study is based on partial DNA sequence information of the mitochondrial cytochrome-b (cyt-b) and the mitochondrial 16S ribosomal RNA genes (16S) and of two nuclear markers: intron 7 of β-fibrinogen (fib-7) and intron 11 of glyceraldehyde 3-phosphate dehydrogenase (GAPDH-11). The main sources of DNA were: (i) tissue or blood samples (stored in alcohol or tissue buffer) plus (ii) a smaller amount of foot pad from study skins. The former were not older than 15 years, the latter up to 130 years.

Results

Alignment length (inclusive indels) of each gene was 838 bp (cyt-b), 836 bp (16S), 473 bp (fib-7), and 288 bp (GAPDH-11), respectively. Thus the overall length of concatenated DNA sequences was 2357 bp. Taking into account the different potential of each of four genes to resolve certain levels of phylogenetic relationships, the respective trees show remarkable congruencies for principal branching patterns. In terms of geographic and taxonomic completeness, the cyt-b tree (Fig. 3) represents the most

Inter- and intra-generic subdivision of Pyrrhula

Our results closely match both the traditional and recent attempts at phylogenetic reconstructions and are also broadly consistent with classic intra-generic taxonomic arrangements. In our data set the Pine Grosbeak Pinicola enucleator appears to be the sister taxon to the genus Pyrrhula as already demonstrated by Arnaíz-Villena et al., 2007, Arnaíz-Villena et al., 2008 who suggested a close relationship between grosbeaks and bullfinches to the genera Leucosticte and Rhodopechys based on cyt-b

Acknowledgments

We are indebted to the following colleagues who supported our work by providing samples, granting access to the collections in their charge and for repeated fruitful discussions on bullfinch phylogeny (in alphabetical order): M.P. Adams, L. Bachmann, E. Bauernfeind, H.-M. Berg, Cheng-Te-Yao, J. Cracraft, B. Däubl, J. Dean, R. Diesener, S. Eck, P. Ericson, J. Fiebig, J. Fjeldså, S. Frahnert, G. Frisk, A. Gamauf, C. Gebhard, H. Heidecke, J. Hegelbach, R. Heleno, A. Hundsdörfer, J.B. Kristensen,

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