ISSN 10623590, Biology Bulletin, 2015, Vol. 42, No. 8, pp. 713–723. © Pleiades Publishing, Inc., 2015. Original Russian Text © V.A. Payevsky, 2015, published in Zoologicheskii Zhurnal, 2015, Vol. 94, No. 2, pp. 221–232.

Taxonomy of True (Fringillidae, Passeriformes): a Review of Problems1 V. A. Payevsky Zoological Institute, Russian Academy of Sciences, St. Petersburg, 199034 Russia email: [email protected] Received February 10, 2014

Abstract—A number of issues in phylogeny and classification of true finches is reviewed. Emphasis is made on poor knowledge of their relationships, in spite of intensive research. The main historic stages of develop ment of true finches classification are reviewed together with the results of molecular studies of their phylog eny. Most recent revisions at the level of subfamilies and genera of true finches are discussed.

Keywords: , , true finches, Fringillidae, , phylogeny, classification DOI: 10.1134/S1062359015080051

1 Avian phylogeny and classification currently state that the limits of the true family are uncer remain hotly debated topics. This debate became tain, and that different and often strongly varying especially acute in conjunction with the advent of views on this topic exist (Sharpe, 1888; Sushkin, 1924; molecular methods in taxonomy. The recent reviews Dementiev, 1937; Tordoff, 1954; Stallcup, 1954; Wet of classification of passerines, Passeriformes (Sibley more, 1960; Kartashev, 1974; Sibley and Ahlquist, and Ahlquist, 1990; Koblik et al., 2014; Payevsky, 1990; Sibley and Monroe, 1990; Cramp and Perrins, 2014), which comprise ca. 60% of extant birds (Sibley 1994; Yuri and Mindell, 2002 etc.). In spite of varying and Monroe, 1990), highlighted ongoing difficulties opinions on individual genera and , based on that taxonomists encounter in defining the family lim both morphological and molecular data, the main dis its in this order. agreements on the limits of taxa have been on the level The family of true finches (Fringillidae) tradition of subfamilies. During the entire history of taxonomy ally includes mainly birds with coneshaped bill, i.e. of true finches, different authors included into or typical seedeaters, with short and stout bill and nine excluded from this family such groups, in whole or functional primary feathers. Structure of palate sur partly, as buntings (Emberizidae), Darwin’s or Gal face with oblong crests, typical of conebilled birds, is apagos finches (Geospizidae), a number of weavers perfected in true finches. This form makes it possible (Ploceidae), in particular true sparrows (genera Passer to shell the seeds by longitudinal movements of sharp Briss., Petronia Kaup, Montifringilla Brehm), cardi mandible edges. True finches are distributed nearly nals (Cardinalidae, or Pyrrhuloxiidae), Hawaiian globally (Eurasia, Africa, North and South America), honeycreepers (Drepanididae), tanagers (Thraupi and their lifestyle is mainly connected with forest veg dae), icterids (Icteridae) and New World warblers etation and scrubland. However, and mountain (Parulidae). Consequently, the number of species in ous species also exist. the family could vary from 137 (e.g. Böhme and Flint, Some true finches are well familiar not only to biol 1994) to 993 (Sibley and Ahlquist, 1990). ogists, but to the general public as well. This family includes such species as chaffinches, goldfinches, The situation is further complicated by semantic siskins, bullfinches, , canaries etc. Many true ambiguities. The English word ‘finch’ and the German finches inhabit parks and gardens close to humans, word ‘Fink’ denote not only true finches, but is used have beautiful ornate plumage and superb vocal quali for more than one thousand species from other fami ties. It is thus somewhat puzzling that in spite of this lies: estrildid finches (Estrildidae), weavers, cardinals, popularity of true finches, their taxonomy and rela Darwin’s finches and some buntings. For this reason, tionships remain poorly studied and in a need of a the English vernacular name for Fringillidae is true revision. finches, and the German authors write of ‘eigentli Most handbooks on birds and taxonomic studies, chen Finken’, i.e. proper finches. At the same time, both from the 19th20th centuries and the recent ones, New World buntings (family Emberizidae) are called American sparrows, which sometimes leads to the 1 The article was translated by the author. ambiguous statement that sparrows are finches.

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All that defines the aims of the current contribu anatomic studies in the 19th century, in particular the tion. They are to follow the controversial history of classic studies by E.H. Haeckel and T.H. Huxley, led to research into phylogeny and classification of true a significant progress in the field of avian systematics. finches and on the basis of recent molecular, morpho An important milestone was the Catalogue of Birds in logical, and biogeographic studies to define the main the British Museum by R.B. Sharpe, which diagnosed points of the current taxonomy of this group. families, subfamilies and genera. The first volume was published in 1874, and in the 12th volume (Sharpe, 1888) true finches included 97 genera and were MAIN STAGES OF HISTORY OF TRUE divided into three subfamilies: Fringillinae, Emberiz FINCHES CLASSIFICATION BEFORE inae and Coccothraustinae. However, the author THE PERIOD OF MOLECULAR STUDIES emphasized that no one had proposed a satisfactory In his classification of , Aristotle (4th century system of true finches. The subfamilies by Sharpe were B.C.) mentioned both insectivorous and herbivorous criticized by Ridgway (1901) as nonnatural groups. birds, and also true finches. Further attempts to con The latter author divided true finches into 18 groups: struct a system of birds, finches including, were based Fringillae, Loxiae, Pyrrhulae, Coccothrausteae etc. on external characters and similarities in body struc In the classic 19th century works on avian system ture, diet and behavior. They were made in publica atics by M. Fürbringer (1888) and H. Gadow (1893), tions of U. Aldrovandi, P. Belon, J. Ray, F. Willoughby, most passerines were considered closely related due to M. Brisson, G. Cuvier, B. Merrem, C.L. Nitzsch, their morphological similarity. Fürbringer lumped C.J. Temminck, J. Cabanis, C.L. Bonaparte, J.G. Gme them into just two families, but Gadow recognized lin, J.B. Lamarck, G.L. Buffon (the reviews: Karta among songbirds (Oscines) 28 families, true finches shev, 1974; Sibley and Ahlquist, 1990). A new era in among them. In his monograph on the birds of the systematics, based on binary taxonomy and hierarchi world, M. A. Menzbier (1909) considered true finches cal system of taxa, was started by the work of Carolus to be close to buntings, however mentioning signifi Linnaeus. In the 10th edition of his ‘Systema Naturae’ cant difference between these two families in jaw (Linnaeus, 1758) class birds and order passerines structure. Following Sharpe, Menzbier included all (Passeres) among species of the Old and the New true sparrows into true finches, but split World include L. with species like into a separate family Coccothraustidae, which also chaffinch, brambling, goldfinch, linnet, , siskin included and cardinals. and serin, currently F. coelebs L., F. montifringilla L., A significant contribution to the systematics of true carduelis (L.), cannabina (L.), finches was made by the studies of P.P. Sushkin. On the Acanthis flammea (L.), spinus (L.), basis of structure of syrinx, bony palate and external canaria (L.), respectively; and genus Loxia L. with morphology of horny palate Sushkin (1924, 1925) species , , bullfinch, and divided true finches into three large groups, Cardue pine , currently L. curvirostra L., Chloris chlo line, and Emberizine. Cardueline consist of ris (L.), pyrrhula (L.), Coccothraustes cocco three lineages with genera: 1—Fringilla L., 2—genera thraustes (L.), Pinicola enucleator (L.), respectively. of cardinals, 3—Carduelis Briss., Carpodacus Kaup After the introduction of a new taxon rank, family, and Coccothraustes Briss. Cardueline are closer related in the early 19th century, the name Fringillidae Leach to PloceoPasserine than to Emberizine, and Hawai 1820 starts to denote true finches. Different classifica ian honeycreepers are particularly close to Cardueline tions of North American birds in 1858–1872 included (Sushkin, 1929). As a result, Sushkin proposed the fol into this family true finches, American buntings lowing taxonomic decisions: superfamily Fringilloidei (= American sparrows), true sparrows and parrotbills consists of families Fringillidae (subfamilies Fringilli (Paradoxornis Gould). Species were distributed across nae, , Cardinalinae), Ploceidae (subfami subfamilies and cohorts mainly on the basis of their lies Passerinae, Viduinae, Ploceinae) and Drepanid external morphology: bill shape, tongue structure, idae, whereas superfamily Emberizoidei consists of number of primaries, form of wings, tail and legs families Icteridae, Coerebidae, Tanagridae and (Kartashev, 1974; Sibley and Ahlquist, 1990). At the Emberizidae. same time, the classification of oscine passerines by By the mid 20th century E. Stresemann (1959) Wallace (1874) was based solely on wing structure, believed that genuine phylogeny could never be stud with true finches lumped into the ‘tanagroid’ group of ied, and thus no classification could be built upon it, 9primaried songbirds together with tanagers and six and that comparative studies had ultimately failed more groups. In a subsequent review (Sclater, 1880), after nearly 200 years of efforts. In spite of this pessi this publication of Wallace was subject to severe criti mistic view, the 1960s saw a new period of debate on cism, in particular for putting true finches and weavers avian systematics, linked with development of cladis into different groups of songbirds, even though they tics and numerical taxonomy. However, the most pop ‘hardly represented distinct families’. ular among ornithologists became the system of Popularization of the evolutionary theory by A. Wetmore. In its final version (Wetmore, 1960) the Charles Darwin and the development of comparative order of passerines was divided into four suborders,

BIOLOGY BULLETIN Vol. 42 No. 8 2015 TAXONOMY OF TRUE FINCHES 715 and the suborder of songbirds (Passeres) consisted of ley and Ahlquist, 1990). In this study the only source 54 families, from larks to true finches. Wetmore’s sys of information on phylogeny used was hybridization of tem was accepted by J.L. Peters in the Checklist of singlestranded DNA, with temperature gradient dur Birds of the World, but in the volumes devoted to pas ing hybridization as a proxy for relatedness. Phyloge serines (Peters, 1951–1986), the sequence of families netic schemes were based on cladistic principles, in by Wetmore was replaced by the socalled Basel particular taxon hierarchy and rank were based on ori sequence which has been accepted at the IOC in Basel gin sequence, with sister groups invariably having in 1954. Passerines there include 38 families, among identical rank. The data on passerines allowed the which true finches are placed along buntings, Hawai authors to confirm the traditional division of the order ian honeycreepers, icterids, estrildid finches and into two suborders—Tyranni, or Suboscines and Pas weavers. seri, or Oscines. The classification of the true finch In the monograph on avian systematics, Kartashev family from the superfamily of Passeroidea, based on (1974), after mentioning that true finch taxonomy is DNA–DNA hybridization, looked as follows: insufficiently developed, lists four subfamilies that Family Fringillidae, true finches: 240 genera, 993 contain 89–123 genera and 414–468 species: bun species tings, Darwin’s finches, cardinals and true finches. Subfamily Peucedraminae: 1 genus, 1 species However, the respected handbook on birds of Western Subfamily Fringillinae, Old World finches: 39 gen Palaearctic (Cramp and Perrins, 1994), following the era, 169 species list of Holarctic birds (Voous, 1977), treats true finches Tribes: Fringillini: 1 genus, 3 species, Carduelini: and buntings as distinct families. 20 genera, 136 species, : 18 genera, 30 species RELATIONSHIPS OF TRUE FINCHES Subfamily Emberizinae, News World 9primaried AS SHOWN BY PROTEIN ELECTROPHORESIS oscines: 200 genera, 823 species The data of protein electrophoresis that is deter Tribes: Emberizini: 32 genera, 156 species, mined by their amino acid structure and sequence Parulini: 25 genera, 115 species, have shown with a some degree of certainty (Sibley, Cardinalini: 13 genera, 42 species, Icterini: 26 gen 1970) that genus Passer deviates from the family of era, 97 species, weavers and might be closer related to true finches Thraupini: 104 genera, 413 species and that genus Fringilla is related to the subfamily of Commentaries to this classification state that the carduelines. Starch gel electrophoresis data showed subfamily Fringillinae originated in the Old World, that among all studied species of North American and Emberizinae—in the New World, and that the cardueline finches, the genus most closely linked to whole family of true finches is a sister group for the genus Carduelis was Loxia and that most speciation clade NectariniidaePasseridae (sunbirdspasserids), events in carduelines occurred between midlate with these lineages splitting some 25–35 million years Pliocene (4 million years b.p.) and mid Pleistocene b.p. (Sibley and Ahlquist, 1990). Soon after the great (500000 years b.p.), but subspecies diverged in late success of these studies, critique on various aspects of Pleistocene. It has been also shown that Loxia curvi this phylogeny started to emerge, topics of passerine rostra and L. leucoptera Gm. are moderately different, taxonomy including (Ericson and Johansson, 2003; whereas Carduelis flammea and C. hornemanni exilipes Barker et al., 2004 etc.). Some authors suggested that (Coues) are genetically similar. A phylogeny of cardu both phylogeny by Sibley and Ahlquist and taxonomy eline finch genera derived from the electrophoretic partially based on it (Sibley and Monroe, 1990), are data generally agreed with the results based on hind rather problematic. However, phylogeny and classifi limb myology. However, the studies of avian systemat cation of passerines with 42 families after Sibley and ics on the basis of electrophoresis and chromatography Ahlquist became the basis for subsequent analyses. did not develop into a major field, because less than 10% of the genome is reflected in the amino acid sequence of proteins. ON COMPOSITION AND TAXONOMIC POSITION OF THE SOCALLED ‘NEW WORLD 9PRIMARIED OSCINES’ PHYLOGENY AND CLASSIFICATION A. R. Wallace was the first author who lumped OF TRUE FINCHES BASED together ‘New World 9primaried oscines’, i.e. song ON DNA–DNA HYBRIDIZATION birds with nine primary feathers, as opposed to passe The first molecularbased studies of passerine phy rines with 10 primaries (Wallace, 1874). He included logeny were published already in the 1980s (e.g. Sibley into this group the families of swallows and martins and Ahlquist, 1982; Bledsoe, 1988). However, a large (Hirundinidae), wagtails and pipits (Motacillidae), scale phylogenetic study of evolution of all birds based waxwings (Bombycillidae), flowerpeckers (Dicae on DNADNA hybridization studies, the first ever, idae), the bananaquit (Coerebidae), New World war was published by Ch. G. Sibley and J. E. Ahlquist (Sib blers, Hawaiian honeycreepers, tanagers, icterids and

BIOLOGY BULLETIN Vol. 42 No. 8 2015 716 PAYEVSKY true finches, American sparrows including. Based on edge of the lower beak (Nekrasov, 1978). However, this DNA hybridization data (Sibley and Ahlquist, 1990), finchlike method of seed handling is used, with slight the subfamily Emberizinae included the aforemen modification, by other conebilled birds as well, e.g. tioned groups, with the exception of swallows and by cardinals, tanagers, Hawaiian honeycreepers, some martins, wagtails and pipits, waxwings and flower American sparrows (= New World buntings) and bun peckers. These authors called the whole this group tings of Eastern Palaearctic, unlike other Old World with a number of others birds ‘clade Fringillidae’. As a buntings (Koblik, 1994, 2007). Therefore, buntings result, many sources started to call the whole family include groups with varying morphology of the rham Fringillidae the ‘New World 9primaried oscines’, photheca, including some birds with finchlike struc which is erroneous, because, first, Fringillidae origi ture and functions. nated in the Old World, and second, this feature is The results of molecular studies are similarly shared by them with other avian families. ambiguous. DNA–DNA hybridization data suggested As already discussed (Yuri and Mindell, 2002; that buntings were a subfamily within true finches Payevsky, 2014), in spite of the continued use of the (Sibley and Ahlquist, 1990). The data on sequencing term ‘New World 9primaried oscines’, many authors the mtDNA Cyt b gene (Groth, 1998) cast doubt on mention that all these birds in fact have 10 primaries, the sister group relationship between Old World but the tenth one (or the first one, if numbered ascen finches and American sparrows and showed that the dantly) is reduced, sometimes to a great extent. There latter are more closely related to wagtails and Old fore a more exact name for this group would be World (= true) sparrows. However, subsequent molec ‘oscines with 9 functional primaries’. In most detail ularbased phylogenetic analyses, also based on the topic of the rudimentary primary was studied by mtDNA sequencing, drew different conclusions. The B.K. Stegmann (1962) who showed that in fact the analysis of 40 taxa of New World 9primaried oscines number of primaries is always 10, but length of one of supported the monophyly of this group and the sister them may vary greatly. The same conclusion was group relationship between true finches and the reached by Hall (2005) on the basis of studying 104 Emberizini clade, which includes American sparrows, bird species. The latter author showed that in the New World warblers, tanagers and cardinals (Klicka extreme cases of reduction the tenth primary (= the et al., 2000). The analysis performed in 44 species of first if numbered ascendantly) is hidden by the covert Old and New World finches (Yuri and Mindell, 2002) of the previous (= next) primary, so that one has to supported monophyly of the family of true finches and raise the covert to see it. The assumption of mono its two subfamilies, Fringillinae and Emberizinae, as phyly of the New World 9primaried oscines is based sister groups. Besides, this analysis confirmed the Old on the lack of the tenth functional primary (Sibley and World origin for true finches. Subfamilies true finches Ahlquist, 1990). However, as this feather is also rudi and buntings within the family of true finches were mentary in swallows, sunbirds, sparrows and silvereyes confirmed by another molecular analysis (Liang et al., (Zosteropidae), this character does not prove mono 2008). A molecular study of phylogeny and classifica phyly (Yuri and Mindell, 2002). tion of Old World buntings (Alström et al., 2008) sup ported its monophyly, but found no sistergroup rela tionship with Emberizini of the New World. Finally, RELATIONSHIP BETWEEN the latest studies (Barker et al., 2013; Cracraft, 2014) TRUE FINCHES AND BUNTINGS found that the voluminous group of New World As shown above, this question has been answered oscines with 9 functional primaries, which includes, variably on the basis of traditional morphological data. following these authors, 12 more families apart from These groups have been assigned different rank, from the buntings and is called the superfamily Emberiz subfamily through family to superfamily. Their mor oidea, is a sister group to the family Fringillidae. phological difference is widely known. Body of most In respect to the relationship between true finches true finches is generally more bulky, and bill is larger and buntings the species of a special taxonomic posi and stouter than in buntings. The ridge of upper beak tion, which combines the characters of both in true finches is straight or convex, and is never and finches, should be mentioned. It is Przevalski’s slightly concave, like in some buntings. In buntings, finch Urocynchramus pylzowi Przevalski 1876 which unlike true finches, with closed bill the middle parts of inhabits mountains in western . This is a bird upper and lower beak do not touch and form a slit, with a long stepped tail, brown plumage with mark because the cutting edge of the upper beak forms a ings, with pink throat, breast and belly in males, which curve; mandibular angle is much more developed in is reminiscent of the longtailed Uragus buntings than in finches. Morphological peculiarities sibiricus (Pall.), by its appearance but has a bunting of true finches in the rhamphotheca structure include like beak. However, the most striking feature of this a high arc of the horny palate, and a system of palate species is its well developed first (or, counting descen crests divided by deep sulci. The main trophic special dantly, tenth) primary, which is in stark contrast to the ization of finches, shelling of seeds, is performed by strongly reduced feather of finches and buntings. This fixing them in the sulci and cutting their coat by the species has been assigned to both these families, but as

BIOLOGY BULLETIN Vol. 42 No. 8 2015 TAXONOMY OF TRUE FINCHES 717 early as 1918 J. Domaniewski proposed the family that of true finches, cardinals and Galapagos finches Urocynchramidae with a single genus and a single spe favored a rank of a distinct family Drepanididae (Kob cies. This viewpoint has been supported by Wolters lik, 1994b). (1979), and later confirmed by molecular studies. Based on the data on electrophoresis of proteins Sequencing its mtDNA showed that Przevalski’s finch different authors obtained controversial results con is not a rosefinch and generally is neither a finch not a cerning a relationship of Hawaiian honeycreepers with bunting. A further study (Yang et al., 2006) confirmed carduelines. Silbley (1970) claimed that his data sup its lack of affinity either to Carpodañus or to Uragus, port this relationship, whereas other authors reported and also to Estrildidae, Ploceidae and Prunellidae. that nine honeycreeper species included in their study The latter authors suggested that family Urocynchra were more closely related to two bunting species than midae is as old as Fringillidae, or older. to two carduelines (Johnson et al., 1989). However, the results of a DNA hybridization study based on comparing DNA of sanguinea Gm. with RELATIONSHIPS DNA of five cardueline species and DNA of the OF HAWAIIAN HONEYCREEPERS chaffinch and 21 other bird species (from buntings, Different sources currently accept 28–32 species of cardinals, tanagers, icterids to thrushes, Old World Hawaiian honeycreepers in 16–20 genera. This group warblers and corvids) showed that Hawaiian honey of birds shows one of the most impressive adaptive creepers have more recent common ancestors with radiations among . They are characterized by cardueline finches than with any other group studied, incredibly variable bills, ranging from short, finchlike and that they diverged in mid Miocene, 15–20 million bills in genera Psittirostra Temm., Melamprosops Casey years b.p. (Sibley and Ahlquist, 1982). et Jac., Oust. and Newt. to parrot The results of mtDNA sequencing confirmed the like bills in Pseudonestor Rotsch. and long curved close relationship between Hawaiian honeycreepers treecreeperlike bills of Licht. and with carduelines on the level of sister groups, and also Temm. This variability forced older taxono at the same level between genus Fringilla and the clade mists to distribute Hawaiian honeycreepers between consisting of carduelines and Hawaiian honeycreepers several passerine families, from true finches to flower (Yuri and Mindell, 2002). Finally, the most recent peckers and honeyeaters (Meliphagidae). After many studies combining nuclear and mitochondrial DNA years of morphological research it became apparent sequencing suggested that Hawaiian honeycreepers that all species of Hawaiian honeycreepers are closely are actually carduelines, because they form a clade related and that evolution of the ancestor species in within this subfamily and are a sister group for Asian different ecological niches on oceanic islands resulted of genus Carpodacus (Lerner et al., 2011; in the current diversity (Amadon, 1950; Sibley and Zuccon et al., 2012; Fig. 1). Therefore, a most close Ahlquist, 1982). affinity of Hawaiian honeycreepers and carduelines, Ancestors and relatives of Hawaiian honeycreepers suggested in the beginning of the last century, is con were looked for in different groups of birds, including firmed by multiple research. buntings, tanagers, icterids, New World warblers and flowerpeckers. The first author to clearly establish the NEOTROPIC GENERA OF EUPHONIAS morphological similarity in skull structure between EUPHONIA DESM. AND CHLOROPHONIAS Hawaiian honeycreepers and true finches was P.P. Sus CHLOROPHONIA BONAP. ARE TRUE FINCHES hkin; he suggested their close affinity to carduelines (Sushkin, 1929). This view was subsequently con In spite of some characters that make them distinct firmed by W. Bock (1960) and R. Raikow (1977). The from other Thraupidae, birds of these two genera were latter author concluded that Hawaiian honeycreepers traditionally treated as tanagers, because with similar are descendants of a single founder cardueline species, appearance and foraging habits they also have bright similar to the extant Psittirostra honeycreeper, and that plumage. Molecular studies of taxonomy of tanagers nectar feeding evolved in the Hawaii in parallel with (Burns, 1997) showed that several genera usually similar developments in other avian families. How included into this group actually form a clade outside ever, an alternative viewpoint exists. The results of of the main stem, which warranted their exclusion studying rhamphotheca and horny palate in four spe from tanagers. This taxonomic decision has been sup cies of seedeating Hawaiian honeycreepers (Loxio ported by several analyses, which suggested that ides bailleui, kona, palmeri, euphonias are a sister group of either Fringilla (Yuri coccinea) showed no traces of finchlike struc and Mindell, 2002) or of Carduelinae, and are their tures in the horny palate and deep specialization of rather specialized form, or a basal radiation not previ beaks of each of these species to narrow trophic ously recognized within the clade of 9primaried niches. It prevents lumping Hawaiian honeycreepers oscines (Klicka et al., 2000), or are placed within Car and true finches into a single subfamily, but does not duelinae (Erikson and Johansson, 2003). rule out a common ancestor. Summarizing, compari A largescale study by a combination of nuclear son of rhamphotheca of Hawaiian honeycreepers with and mitochondrial DNA sequencing that included ten

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Fringilla coelebs Fringilla montifringilla Chaffinch, Brambling Chlorophonia cyanea Euphonia musica Euphonia chlorotica Euphonia finschi Euphonia xanthogaster Euphonias Euphonia cayennensis Euphonia rufiventris Euphonia minuta Euphonia laniirostris Euphonia violacea carnipes vespertina Coccothraustes coccothraustes Hawfinch migratoria montana Hawwaiian Loxioides bailleui Hemignathus virens honeycreepers Erythrina (Carpodacus) erythrina Haematospiza sipahi Carpodacus (Chaunoproctus) ferreorostris Carpodacus rubicilla Carpodacus rubicilloides Carpodacus rhodochlamys Carpodacus pulcherrimus Carpodacus rodochrous Rosefinches Carpodacus rodopeplus Carpodacus vinaceus Carpodacus synoicus Carpodacus (Kozlowia) roborowskii Carpodacus (Uragus) sibiricus Carpodacus roseus Carpodacus thura Carpodacus puniceus Carpodacus (Pinicola) subhimachala

Fig. 1. Cladogram of relationships within subfamilies Fringillinae, Euphoniinae and three tribes from the subfamily (Cocco thraustini, Drepanidini and Carpodacini), based on combined data of sequencing nuclear and mitochondrial DNA. Simplified from: Zuccon et al., 2012, with alterations.

South American euphonia species (Zuccon et al., (goldfinches, siskins, greenfinches and linnets), based 2012) made it possible to identify three well supported on sequencing of the mitochondrial Cyt b gene, clades at the level of subfamilies: Fringillinae, Eupho showed that very rapid speciation in this subfamily niinae and Carduelinae (Fig. 1). Euphonias are rather occurred in the late Miocene and Pliocene (9–2 mil distinct from other true finches. Apart from difference lion years b.p.) in both northern and southern hemi in plumage, they are primarily not seedeaters but fru spheres. The Pleistocene ice ages played no decisive givores, and also feed their young by fruits. Their nests role in the origin of the current specific diversity and have a side entrance and not an open cup, as nests of could only have contributed to the development of true finches. Presence of such South American tropi subspecies (ArnaizVillena et al., 1998). The same cal clade inside the true finch family, most members of data suggest that North American carduelines should which inhabit the Old World, suggests an ancient be called siskins, and not goldfinches, because they are intercontinental dispersal and subsequent radiation only distantly related to the . Fur (Zuccon et al., 2012). ther studies (ArnaizVillena et al., 2007a; 2012) made it possible to identify three distinct and parallel evolu tionary radiations of American siskins that have been PHYLOGENY OF CARDUELINE treated as members of genus Carduelis and that have FINCHES (CARDUELINAE) originated in the recent 5 million years: 1—North Cardueline finches are the most numerous group of American one, consisting of C. dominicensis Bryant, true finches (183 species) with a global distribution. C. atriceps (Salv.), C. pinus (Wils.), C. pinus perplexus Their phylogeny and phylogeography in the recent (van Ross.) and C. spinus (L.), as their ancestor, (2) years has been a subject of intensive research by Middle American one, consisting of C. tristis (L.), molecular methods. A series of contributions by Span C. psaltria Say, C. lawrencei Cass., and (3) South ish authors (ArnaizVillena and coauthors) in 1998– American one of C. atrata d’Orb. et Lafr., C. crassiros 2012, and other significant publications (van den tris (Land.), C. spinescens (Bonap.), C. cucullata Elzen, 2000; Nguembock et al., 2009; Töpfer et al., Swain., C. yarrelli Audub., C. magellanica (Vieill.), 2011; Zuccon et al., 2012; Tietze et al., 2013) have C. olivacea (Berl. Et Stolz.), C. xanthogastra (Du Bus), considerably altered our idea of phylogeny and classi C. barbata (Mol.) and C. notata Du Bus. All three radi fication of this subfamily. ations are genetically related to linnet and Phylogenetic analysis of four groups of species, (C. flavirostris (L.)), but their common ancestor is not sometimes lumped into the single genus Carduelis known. These authors believe that

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C. spinus could have been the ancestor of the North (Gm.) and C. mexicanus Müll., as compared to Eur American radiation, because it is clearly genetically asian ones, C. erythrinus (Pall.), C. roseus (Pall.), related to some species and could have reach America C. rubicilloides Przev., C. thura Bonap. et Schl., C. tri through Beringia. It could have reached the Antilles fasciatus Verr., belong to a different lineage (Arnaiz during the Pliocene and evolved into Villena et al., 2007). This decision was supported sub (C. dominicensis), that gave rise to sequently, therefore for American rosefinches the res (C. pinus) which is a sister taxon for C. spinus. More urrected generic name Haemorhous Swain. was sug over, it is believed that C. notata, which currently gested (Zuccon et al., 2012). inhabits Mexican highlands, gave start to the whole A number of species from genera Carpodacus, South American radiation some 3 million years b.p. It Cab. and Leucosticte Swain. that exist in is also suggested that this evolution was mainly driven extreme conditions, in and high mountains, by sexual selection (van den Elzen et al., 2001). are genetically different from congenerics that inhabit Largescales analyses based on sequencing more benign environments (ArnaizVillena et al., mtDNA and nuclear DNA suggest (ArnaizVillena et 2008). For instance, genus mountain finches Leucos al., 2001; Nguembock et al., 2009; Zuccon et al., ticte includes taxa adapted to cold climates that live in 2012) that three largest genera of this subfamily, Car the mountains of Altay, Sayan, Tien Shan, Himalayas duelis, Carpodacus and Serinus Koch, into which up to above the treeline, and in North American rocks and 70% of its species were traditionally lumped, are actu mountains. All mountain finches are in the tribe Pyr ally polyphyletic, which greatly hampers interpreta rhulini. Cyt b gene sequencing data suggest that Asian tion of their evolution. As a result, the following solu and graycrowned rosy finches, and tion was proposed (Nguembock et al., 2009, Zuccon , and also darkbreasted rosefinch et al., 2012): genus Carduelis is limited to just two spe form a single lineage of aridzone finches. Even cies, European goldfinch (grayheaded goldfinch, though this group includes species that differ by their C. caniceps Vig., is without species status) and citril morphology, structure, plumage, environment and lif finch, C. citrinella (Pall.). Siskins, greenfinches, lin estyle, all these species are genetically related and may nets and form distinct clades, therefore they be lumped in the tribe Pyrrhulini (ArnaizVillena are given their old generic names, Spinus Koch for et al., 2014). siskins, Chloris Cuv. for greenfinches, Linaria Bechst. The latest molecular analysis (Zuccon et al., 2012) for linnets, Acanthis Bork. for redpolls, which com showed that the genus Carpodacus should include the pletely agrees with traditional morphologybased tax longtailed rosefinch, the crimsonbrowed finch Pini onomy (Wolters, 1982). However, all South American cola subhimachala (Hodg,), the extinct Bonin gros siskins have been given the resurrected generic name beak Chaunoproctus ferreorostris (Vig.) and the Sporagra Reichen. (Fig. 2) by the South American Clas Roborovski’s Rosefinch Kozlowia roborowskii Przev. sification Committee of the AOU, even though it is based However, the darkbreasted rosefinch may be trans on weakly supported data (Nguembock et al., 2009). ferred in the resurrected monotypic genus Procardue Phylogenetic relationships between different gen lis Blyth, and for Blanford’s rosefinch Carpodacus era of carduelines, based on mtDNA sequencing, rubescens (Blanf.), which also forms a distinct lineage, showed the following (ArnaizVillena et al., 2001). the monotypic genus Agraphospiza gen. n., is sug Crossbills appeared to be closely related to redpolls. gested. Both these genera belong to Pyrrhulini. Scarlet is not related to crossbills and rosefinch C. erythrinus (Pall.) is not included into the rosefinches, as assumed earlier, but most probably has main rosefinch clade, and for it the old generic name a common ancestor with bullfinches, with which it Erythrina Brehm is suggested (Fig. 1). diverged 11 million years b.p. Hawfinch in this paper The rather large specific diversity of serins and considered to be a clade isolated from all other genera canaries Serinus Koch is limited to Africa and the studied, but in the next publication it was presented as Mediterranean, with the exception of two species. a close relative of Eurasian (Eophona Gould Sequencing Cyt b gene from 20 species of this genus and Mycerobas Cab.). The same result was obtained by (ArnaizVillena et al., 1999) showed just ca. 4% of the combination of nuclear and mitochondrial DNA genetic divergence between species, which suggest sequencing (Zuccon et al., 2012): hawfinch, these rapid radiation. Molecular data together with biogeo grosbeaks and the genus Hesperiphona Bonap. form a graphic information and data on body size allowed the welldefined clade within Carduelinae (Fig. 1). authors to group Serinus species into five clusters: 1— Carpodacus rosefinches are a large group of Hol Mediterranean: S. canaria (L.). 2—middlesized arctic species with a diversity hotspot in the Hima African and Asian: S. alario (L.), S. canicollis layan region. An analysis of their relationships (Swain.), S. pusillus (Pall.); 3—small African: (ArnaizVillena et al., 2001) showed that most S. mozambicus Müll., S. leucopygius (Sund.), rosefinches are closer to Carduelis species than other S. atrogularis (Smith), S. citrinipectus Clan. et Law true finches, and only the darkbreasted rosefinch son, S. dorsostriatus (Reich.), S. citrinelloides Rüpp.; C. nipalensis (Hodgs.) is sharply different. North 4—large African: S. sulphuratus (L.), S. albogularis American rosefinches C. cassinii Baird, C. purpureus (Smith), S. flaviventris (Swain.), S. gularis (Smith)

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Pinicola enucleator Pyrrhula nipalensis Pyrrhula erythaca Pyrrhula pyrrhula Rhodopechys sanguineus githagineus Bucanetes mongolicus Agraphospiza (Carpodacus) rubescens Bullfinches, Callacanthis burtoni Pyrrhoplectes epauletta Procarduelis (Carpodacus) nipalensis Leucosticte nemoricola Leucosticte brandti Leucosticte arctoa Leucosticte tephrocotis Haemorhous (Carpodacus) mexicanus American Haemorhous (Carpodacus) purpureus rosefinches Rhodospiza obsoleta Rhynchostruthus socotranus Chloris (Carduelis) chloris Chloris (Carduelis) sinica Greenfinches Chloris (Carduelis) ambigua Chloris (Carduelis) monguilloti Chloris (Carduelis) spinoides Linurgus olivaceus (Serinus) mennelli Crithagra (Serinus) sulphuratus African canaries Crithagra (Serinus) burtoni and Crithagra (Serinus) striolatus seedeaters Crithagra (Serinus) rufobrunneus Crithagra (Serinus) citrinelloides Crithagra (Serinus) leucopygius Crithagra (Serinus) mozambicus Linaria (Carduelis) cannabina Linaria (Carduelis) flavirostris Linnets Acanthis (Carduelis) flammea Redpolls Acanthis (Carduelis) hornemanni Loxia leucoptera Crossbills Loxia curvirostra Loxia pytyopsittacus Chrysocorythus (Serinus) estherae Carduelis carduelis Goldfinches Carduelis citrinella Serinus canaria Serinus serinus Serinus canicollis Serins Serinus pusillus Serinus syriacus Spinus (Serinus) thibetanus Spinus (Carduelis) tristis Spinus (Carduelis) psaltria Siskins Spinus (Carduelis) pinus Spinus (Carduelis) spinus Sporagra (Carduelis) barbata Sporagra (Carduelis) cucullata Siskins Sporagra (Carduelis) atrata of South America Sporagra (Carduelis) magellanica

Fig. 2. Cladogram of relationships within tribes Pyrrhulini and Carduelini, based on combined data of sequencing nuclear and mitochondrial DNA. Simplified from: Zuccon et al., 2012, with alterations. Continued from Fig. 1.

BIOLOGY BULLETIN Vol. 42 No. 8 2015 TAXONOMY OF TRUE FINCHES 721 and 5—relict: S. thibetanus (Hume), S. striolatus current classification of true finches may be suggested, Rüpp. The subsequent revision of the taxonomy of taking all this into account: African species with isolation of three clades (Nguem Family Fringillidae Leach 1820—true finches, 56 bock et al., 2009) was subject to criticism due to para genera, 218 species phyletic origin of these groups. Novel molecular anal Subfamily Fringillinae Leach 1820—chaffinches yses (Zuccon et al., 2012) showed that genus Serinus and brambling, 1 genus, 3 species should include just six species ( alario, canaria, cani Subfamily Euphoniinae Cabanis 1847—euphonias and ), and for the others collis, pusillus, serinus syriacus and chlorophonias, 2 genera, 32 species that form a monophyletic clade, the resurrected generic name Crithagra Swain. is suggested (Fig. 2). Subfamily Carduelinae Vigors 1825—cardueline finches and Hawaiian honeycreepers, 53 genera, 183 This review shows that controversial pattern of species phylogeny of true finches and actually of the whole Tribe Coccothraustini Swainson 1831—hawfinch passerine order is mainly related to the lack of distinct and grosbeaks, 4 genera, 9 species characters typical of specific groups. This agrees with the pattern of rapid radiation and frequent parallel or Tribe Carpodacini Bonaparte 1854—rosefinches convergent evolution. Since the first monograph on and Bonin grosbeak, 2 genera, 25 species the results of largescale research into avian phylogeny Tribe Drepanidini Cabanis 1847—Hawaiian hon on the basis of DNA–DNA hybridization (Sibley and eycreepers, 22 genera, 33 species Ahlquist, 1990), a lot of molecular studies were pub Tribe Pyrrhulini Vigors 1825—bullfinches, trum lished that much improved our understanding of rela peter finches, pine grosbeak, crimsonwinged finch, tionships within birds, true finches including. Some mountain finches, 9 genera, 22 species novel results from the viewpoint of traditional mor Tribe Carduelini Vigors 1825—goldfinches, phologybased taxonomy may be viewed as not just siskins, greenfinches, linnets, redpolls, crossbills, surprising, but obviously erroneous, especially when serins and canaries, 16 genera, 94 species different molecular data on the same taxon disagree. However, the framework of a impartial review dictated refraining from open polemics. 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