A molecular phylogeny of bullfinches Pyrrhula Brisson, 1760 (Aves: Fringillidae)☆
Graphical abstract
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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,
References (90)
- et al.
Patchy distributions belie morphological and genetic homogeneity in rosy-finches
Mol. Phylogenet. Evol.
(2009) - et al.
Phylogeographic patterns in widespread corvid birds
Mol. Phyl. Evol.
(2007) - et al.
Molecular clocks: when times are a-changin’
Trends Genet.
(2006) - et al.
40Ar/39Ar ages and paleomagnetism of Sao Miguel lavas, Azores
Earth Planet. Sci. Lett.
(1998) - et al.
Rates of cooling and denudation of the Early Penglai Orogeny, Taiwan, as assessed by fission-track constraints
Tectonophysics
(2000) - et al.
New evidence for the age of the Bering Strait
Quartern. Sci. Rev.
(2001) - et al.
Low support for separate species within the redpoll complex (Carduelis flammea–hornemanni–cabaret) from analyses of mtDNA and microsatellite markers
Mol. Phyl. Evol.
(2008) - et al.
Molecular phylogeny of Carduelinae (Aves, Passeriformes, Fringillidae) proves polyphyletic origin of the genera Serinus and Carduelis and suggests redefined species limits
Mol. Phyl. Evol.
(2009) - et al.
Calibration of a molecular clock in tits (Paridae) - do nucleotide substitution rates of mitochondrial genes deviate from the 2% rule?
Mol. Phylogenet. Evol.
(2007) - et al.
Phylogeny of long-tailed tits and allies inferred from mitochondrial and nuclear markers (Aves: Passeriformes, Aegithalidae)
Mol. Phyl. Evol.
(2010)
The utility of DNA sequences of an intron from the β-fibrinogen gene in phylogenetic analysis of woodpeckers (Aves: Picidae)
Mol. Phyl. Evol.
Molecular phylogeny of songbirds (Passeriformes) inferred from mitochondrial 16S ribosomal RNA gene sequences
Mol. Phyl. Evol.
The Pliocene-Pleistocene boundary
Episodes
Handbook of the Birds of India and Pakistan, vol. 10
Phylogeography of crossbills, bullfinches, grosbeaks, and rosefinches
Cell. Mol. Life Sci.
Bayesian phylogeny of Fringillinae birds: status of the singular African oriole finch Lingurus olivaceus and evolution and heterogeneity of the genus Carpodacus
Acta Zool. Sinica
Mitochondrial DNA phylogenetic definition of a group of “Arid Zone” Carduelini Finches
Open Ornithol. J.
The Azores Bullfinch -Pyrrhula murina Godman, 1866. The history of a bird species: persecuted - missing - rediscovered - protected (?)
Ann. Naturhist. Mus. Wien
Studies of West Palearctic Birds 191. Azores Bullfinch (Pyrrhula murina)
Brit. Birds
Unusual sperm morphology in the Eurasian bullfinch Pyrrhula pyrrhula
Auk
Ultrastructure of the unusual spermatozoon of the Eurasian bullfinch (Pyrrhula pyrrhula)
Acta Zool.
Finches and Sparrows
TCS: a computer program to estimate gene genealogies
Mol. Ecol.
The Clements Checklist of Birds of the World
A multilocus study of pine grosbeak phylogeography supports the pattern of greater intercontinental divergence in Holarctic boreal forest birds than in birds inhabiting other high-latitude habitats
J. Biogeogr.
BEAST: Bayesian evolutionary analysis by sampling trees”
BMC Evol. Biol.
Relaxed Phylogenetics and Dating with Confidence
PLoS Biol.
The unusual sperm morphology of the Eurasian Bullfinch (Pyrrhula pyrrhula) is not due to the phenotypic result of genetic reduction
Auk
Mitochondrial resolution of a deep branch in the genealogical tree for perching birds
Proc. R. Soc. Lond. B
Confidence limits on phylogenies: an approach using the bootstrap
Evolution
Sapayoa aenigma: a New World representative of ‘Old World suboscines’
Proc. R. Soc. Lond. B
Evolution on a volcanic conveyor belt: using phylogeographic reconstructions and K-Ar based ages of the Hawaiian Islands to estimate molecular evolutionary rates
Mol. Ecol.
Mid-Pleistocene divergence of Cuban and North American ivory-billed woodpeckers
Biol. Lett.
Is there a universal mtDNA clock for birds?
J. Avian Biol.
Phylogeny of titmice (Paridae): II. Species relationships based on sequences of the mitochondrial cytochrome b gene
Auk
Latitude, elevation and the tempo of molecular evolution in mammals
Proc. R. Soc. Lond. B
BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT
Nucl. Acids. Symp. Ser.
The complete sequence of the mitochondrial genome of Buteo buteo (Aves, Accipitridae) indicates an early split in the phylogeny of raptors
Mol. Biol. Evol.
Signature of ancient population growth in a low resolution mitochondrial DNA mismatch distribution
Hum. Biol.
Die Vögel der paläarktischen Fauna, vol. 1, issue 1
The Cenozoic History of Beringia–A synthesis
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Strict allopatric speciation of sky island Pyrrhula erythaca species complex
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Transverse Alpine Speciation Driven by Glaciation
2016, Trends in Ecology and EvolutionGenetic and morphometric diversity of the goldcrest (Regulus regulus) populations in the Azores
2014, ZoologyCitation Excerpt :These islands are discrete, well-defined, geographic entities with reduced gene flow and lower species diversity when compared with continental areas. Recently, three studies focusing on the genetic diversity and phylogeography of Azorean passerines revealed significant genetic differences in several species in relation to populations from continental areas and/or other Atlantic island archipelagos: (i) Töpfer et al. (2010) assigned species status to the Azorean bullfinch (Pyrrhula murina) from São Miguel, (ii) Neves et al. (2010) identified a significant genetic difference between starlings (Sturnus vulgaris) from the Azores and other European populations, and (iii) Rodrigues et al. (2014) showed that chaffinches (Fringilla coelebs) were genetically similar among the nine islands of the Azores but significantly different from chaffinches on the Canary Islands, Madeira, and Western Europe. Conversely, several studies revealed a small or no genetic difference from other populations, namely canaries (Serinus canaria) (Dietzen et al., 2006), blackcaps (Sylvia atricapilla) (Dietzen et al., 2008), and robins (Erithacus rubecula) (Rodrigues et al., 2013), suggesting that colonisation of the Azores by these species took place relatively recently.
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2012, Quaternary Science ReviewsCitation Excerpt :The range of geological ages of the macaronesian islands is considerable (0.25–29 my) and so therefore is the range of possible colonization dates for the avifauna. However, recent studies estimating genetic divergence between island and continental lineages suggest a mainly a Pleistocene (0.01–2.6 my) colonization of Macaronesia (Voelker, 1999; Idaghdour et al., 2004; Päckert et al., 2006; Illera et al., 2008a; Töpfer et al., 2011), but with some Pliocene (3–4 my) (Dietzen et al., 2006; Illera et al., 2011) and Holocene (<0.01 my; Pérez-Tris et al., 2004; Dietzen et al., 2008) elements (Fig. 2; S-Table 2). These results contrast with the early to mid Miocene colonization dates (17–20 my) estimated for lizards (Cox et al., 2010), and skinks (Carranza et al., 2008), geckos (Carranza et al., 2002) and invertebrates (e.g. Emerson and Oromí, 2005; Contreras-Díaz et al., 2007) respectively.
The phylogenetic relationships and generic limits of finches (Fringillidae)
2012, Molecular Phylogenetics and EvolutionCitation Excerpt :More recently, analyses based on DNA hybridization (Sibley and Ahlquist, 1990) and sequence data (Arnaiz-Villena et al., 2001; Yuri and Mindell, 2002; Van der Meij et al., 2005; Nguembock et al., 2009) have confirmed the position of Fringilla as the sister lineage to the Carduelinae. The phylogenetic relationships among the cardueline finches have now been examined using morphological (van den Elzen and Khoury, 1999; van den Elzen, 2000; Chu, 2002; James, 2004) and molecular data (Arnaiz-Villena et al., 1998, 1999, 2001; van den Elzen et al., 2001; Ryan et al., 2004; Yang et al., 2006; Nguembock et al., 2009; Töpfer et al., 2011). The molecular studies have suffered from limited taxon sampling, but nonetheless their results are largely congruent and a common pattern emerges.
Speciation and population divergence in a mutualistic seed dispersing bird
2022, Communications Biology
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Results of the Himalaya expedition of J. Martens, No. 271. For No. 270, see Genus (Wrocław) 21 (2010), 319–323.