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ISSN 20790864, Biology Bulletin Reviews, 2014, Vol. 4, No. 2, pp. 143–156. © Pleiades Publishing, Ltd., 2014. Original Russian Text © V.A. Payevsky, 2013, published in Uspekhi Sovremennoi Biologii, 2013, Vol. 133, No. 4, pp. 401–416.

Phylogeny and Classification of , Passeriformes V. A. Payevsky Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg, 199034 Russia email: [email protected]

Abstract—The paper presents an overview of the current state of studying the phylogeny and of the largest taxonomic group of birds—the Passeriformes. Phylogenetic relationships and problems of the classification of according to the data of morphological and molecular studies are discussed. All the results on this issue obtained during the past 25 are considered and summarized.

Keywords: Passeriformes, passerines, diversification, classification, molecular studies, phylogeny, evolution DOI: 10.1134/S2079086414020054

INTRODUCTION are there so many kinds of passerine birds?” The arti cle evoked numerous responses, and soon the issues of Among all the existing organisms, the of birds phylogeny and evolution of passerine birds become is one of the most studied. Nevertheless, their origin, very popular among ornithologists. And because of the phylogeny, and are the subject of endur ing and heated debates, which have significantly mul rapid advances in the molecular research methods, as tiplied due to the use of molecular data. In our time, well as the intensive development in the paleobiogeo birds become a model for the development of the graphical research, many publications on the sub methodology in studying phylogeny (Sibley ject of their origin, adaptive radiation, and diversifica and Ahlquist, 1990; Groth and Barrowclough, 1999; tion rate have appeared. Such an intensification of Cracraft, 2001; Kurochkin, 2006). study over the past 25 years has led to new ideas and a radical revision of the traditional views on the evolu The greatest diversity among currently living birds tion of birds, including passerines. The purpose of this belongs to the order of passerine birds, or Passeri publication is to lead a review of the milestones and formes. This order consists of about 5740 , or results from the study of evolution, phylogeny, and 59% of all living species of birds, that is, of 9672 spe classification of passerine birds. cies in 2057 genera (Sibley and Monroe, 1990). Vari able in structure, ecology, and behavior, passerines widely inhabit all terrestrial biotopes on all continents HISTORICAL MILESTONES except the Antarctica ices. Passerines are so numer OF PASSERINE CLASSIFICATION ous, both in terms of the number of species and the BEFORE MOLECULAR RESEARCH number of populations in nature, that ornithologists in their daily work usually divide all the birds into passe Morphologically, passerines are a very homoge rine and nonpasserines. neous group, and historically it was assumed that pas Most passerines are birds of a small size. The small serines are a monophyletic group. Now their mono est of them, weighing 4–6 g, are the (Regu phyly is well established, both on morphological lus regulus), the (Psaltriparus mini (Raikow, 1986) and molecular basis (Sibley and Ahl mus), and some ( ), the largest, quist, 1990). Nevertheless, the of passe weighing up to 1.5 kg, are the ( rines is a hypothesis, like many other hypotheses of corax) and (Menura superba). They feed phylogeny. The key point of progress in the systematics mainly on , , annelids, seeds, fruit, and in recent years was the awareness of the importance of nectar. The species associated with forests and bushes the tested monophyletic hypotheses (Raikow and dominate; they are the most numerous and diverse in Bledsoe, 2000). Inside the order of passerines, the tropical forests. Because of their vast diversity, relative phylogenetic relationships are very confusing, because ease of observation, and field studies, including col most of the evolutionary lineages occurred through lecting, passerines have long attracted the attention of very rapid radiation during the . As a result a wide range of biologists, from taxonomists and evo of the rapid diversification, there was no possibility of lutionists to ecologists to experimenters. acquiring synapomorphies, which led to unclear In 1986, the American ornithologist Raikow (1986) delineated groups that complicate the reconstruction published an article with the stimulating title, “Why of phylogeny (Lanyon, 1988; Feduccia, 1995).

143 144 PAYEVSKY

The attempts to construct a classification of birds The classifications of birds in the 20th century were based only on certain external traits of the body struc predominantly based on the classical works of Für ture, such as the shape of the bill and other obvious bringer (1888) and Gadow (1893), many provisions of morphological differences (Gray, 1869–1871), did not which, based on reasoning about phylogenetic rela lead to significant advances in the of birds, tionships between taxa, have survived to the present including passerines. Among passerines, there are day. In the classification of birds by Sharpe (1901– many unrelated but morphologically very similar 1909), two groups of passerines—broadbills (Eury ecotypes on different continents, evolved through laimi) and , or primitive passerines convergence, as well as species that are related but (Menurae)—were elevated to the rank of orders, completely dissimilar in appearance. This fact has along with the order of the rest of passerines. The latter always made it difficult to construct a natural system. was divided into two suborders: Mesomyodi, with In the tenth edition of the Systema Naturae of Lin 12 families, and Acromyodi, with 48 families. In the naeus (1758), the class of birds already has the order of system of birds by Wetmore, since 1930 (the latest edi passerines (Ordo Passeres), although it also lists doves tion: Wetmore, 1960), whose classification has been (genus ) and (genus Caprimulgus), acknowledged by many ornithologists and still contin and some passerines are attributed to other orders: ues to be widely used, all Passeriformes were divided genera Corvus, Sitta, and —to into four suborders: broadbills; lyrebirds, or primitive (Picae), as well as (Laniidae)—to Accipitres passerines; ; and oscines (Passeres). The same (Sibley and Ahlquist, 1990). A detailed chronological division was accepted in the subsequently proposed overview of the classification of passerines (Sibley, system (Mayr and Amadon, 1951), although in the 1970; Sibley and Ahlquist, 1990) clearly showed the suborder of oscines the number of families was difficulties of previous taxonomists in determining the changed significantly. Thus, the flycatchers boundaries of the passerine families. The authors of (Muscicapidae), for example, besides flycatchers, also the 19th century classical works on the taxonomy of included , thrushes (Turdidae), bubblers birds (Fürbringer, 1888; Gadow, 1893) were misled by (Timaliidae), (Troglodytidae), and the morphological similarity within the order, espe (Cinclidae). Subsequently, as a result of many studies cially among passerine , forcing them to (Olson, 1971; Sibley, 1974; Feduccia, 1975; Raikow, consider most passerines as closely related species. 1987, etc.), lyrebirds in terms of a number of One can regard a gradual increase in the number of logical features were found to belong to songbirds families of passerines in the taxonomical works as a (Oscines), and broadbills and Tyranni were combined characteristic reflection of overcoming such an into the suborder of Suboscines, although broadbills approach. Fürbringer (1888) distinguished only two differ from the rest of suboscines by significant mor passerine families, but its number in the works of the phological features. subsequent authors was: 35 (Gadow, 1893), 50 (Mayr The Wetmore classification was used by Peters in and Amadon, 1951), 60 (Sharpe, 1901–1909), 63 the of the World, but in the last volumes (Stresemann, 1934), 70 (Wetmore, 1960), 72 (Karta devoted to passerines (Peters, 1951–1986) the shev, 1974), 96 (Dickinson, 2003), and 104 families sequence of the Wetmore families was replaced by the (Wolters, 1975–1982). socalled Basel Sequence adopted at the 11th Interna The division of passerines into groups of songbirds, tional Ornithological Congress in 1954. This list rep or oscines (or suborder Passeri), and suboscines resents passerines as 38 families, among which the (Clamatores, or suborder Tyranni) began in the late of flycatchers also included, like in Mayr and 19th century (Sharpe, 1877–1890; Gadow, 1893). The Amadon (1951), all Sylviidae, Turdidae, and Timali species diversity in oscines is much more than that of idae, and the family of buntings (Emberizidae) suboscines; oscines make up almost half of all modern included, besides buntings, cardinals (Pyrrhuloxiinae) species in the class of birds and represent the largest and (Thraupidae). This sequence of the pas radiation of birds. These two groups, considered most serine families (Mayr and Greenway, 1956) begins often as suborders, differ morphologically, primarily in with (Alaudidae) and (Hirundinidae) terms of structural features of the , the vocal and ends with birdsofparadise (Paradisaeidae) and organ located at the base of a trachea, at the spot of its corvids (). divergence into bronchi. The presence or absence of The Basel Sequence did not satisfy everyone, and specific internal muscles and cartilages and their loca many ornithologists have continued to use the Wet tion characterizes different types of syringes. In more system. Of course, the sequence of taxa in any oscines, the syrinx has a complex morphological classification can hardly speak about real relations structure, which provides their complex vocalization, between the groups in terms of time and kinship, so the while in suboscines it has a less developed structure, order of the listing reflects not so much the passerine leading to simple vocalization. In addition, all subos phylogeny as the convenience for ornithologists. cines, unlike oscines, are characterized by a bulbar However, the pessimism expressed by Stresemann form of the middle ear bone (Ames, 1971; Raikow and (1959) that the true phylogeny, and the classification Bledsoe, 2000). that reflects it, is impossible in principle did not stop

BIOLOGY BULLETIN REVIEWS Vol. 4 No. 2 2014 PHYLOGENY AND CLASSIFICATION OF PASSERINE BIRDS, PASSERIFORMES 145 the intensive research of the evolution and systematics assigned with the same rank. The principles of the sub of birds. ordination of taxa were established in accordance with In the first attempt of a phylogenetic classification the time of their historical origin, being manifested by of the higher taxa of birds (Cracraft, 1981), the entire a hybridization distance indicator of ΔT50H, where T50 class of birds was represented by 20 orders in 9 sec is the temperature in degrees of Celsius in an ideal nor tions. In the last, the ninth section consisted of four malized cumulative frequency of distribution, at orders—Passeriformes, , Coliiformes, which 50% of all potentially hybrid singlecopy DNA and . The proximity of Passeriformes with sequences are in a hybrid form, while 50% are sepa Piciformes and Coraciiformes, as was shown by fur rated. At that, ΔT50H = 1.0 corresponded to 4.5 mil ther research (including in terms of the molecular lion years of evolution, which was calibrated on the data), was fully reasoned. basis of the evolution of passerine birds, where the Δ In the 1960s–1970s there began studies of the phy indicator of the order T50H = 20–22. For construct logeny of birds according to features of the distribution ing dendrograms, Sibley and Ahlquist used the special of proteins in using electrophoresis. The results programs FITCH and KITSCH, the first of which dis concerning passerines (Sibley, 1970) showed with played both a branching pattern and a scale of differ some probability, in particular, that: (1) corvids and ences between taxa reflected in the length of the shrikes (Laniidae) are related, (2) the genera Psaltri branches. This monograph provided the basis and ref and are closely related and are closer erence point for numerous subsequent analyses of the to Sylviidae than to tits (Paridae), (3) the families , not the least of which were of pas Sylviidae and Muscicapidae are closely related and are serine birds, both in terms of the historical aspects of quite close to family of thrushes, (4) the family of sun their formation and their subsequent diversification birds (Nectariniidae) and (Meliphagidae) (Barraclough et al., 1995; Cardillo, 1999; Ericson differ sharply and are not related, (5) the genus of true et al., 2000, 2002, 2003; Cracraft, 2001; Irestedt et al., sparrows () differs from the family of weavers 2001; Ricklefs, 2003, 2006; Barker et al., 2004). () and may be closer to (Fring In the new classification, using the results of DNA illidae), (6) the genus of finches () is closely hybridization, Sibley and Ahlquist (1990) created a related to the subfamily of cardueline finches (Cardu superorder of Passerimorphae, which includes, elinae). besides Passeriformes, the orders of Columbiformes, , and Ciconiiformes, and all Passeriformes PHYLOGENY AND CLASSIFICATION were departed from this of nonpasserines. Also, OF PASSERINES BY DNA HYBRIDIZATION a parvclass Passerae was formed, which included, besides the superorder asserimorphae, the orders of Prior to the 1980s, basic research of the phylogeny (Strigiformes), (Musophagiformes), of birds was based only on morphological traits. Due to (Trochiliformes), swifts (Apodi advances in and research tech formes), (Psittaciformes), and niques, the first attempts using molecular methods for (Cuculiformes) (Fig. 1). solving problems in the systematics of birds had already been taken in 1960s–1970s, and the first sig The data on the phylogeny of passerines allowed nificant results on DNA hybridization were published Sibley and Ahlquist (1990) to confirm the traditional only in the early 1980s (Sibley and Ahlquist, 1983, division of passerines into two suborders—Tyranni for 1985). suboscine passerines and Passeri for oscine passerines. A largescale phylogenetic picture of the evolution These two groups were clearly different in terms of the of birds, the first in the history of taxonomy, appeared measures of DNA–DNA distances, in addition to the in the fundamental book of Sibley and Ahlquist morphological differences,. However, Sibley and Ahl (1990). Based on molecular data, it shows the results quist hypothesized that many oscines of the Austra of the work of numerous researchers on hybridization lia–New Guinea region form a monophyletic of the DNA from 1700 bird species from 168 families, group—the parvorder , which is a sister group where the DNA of each species was crossed in a series to all the remaining oscines forming a monophyletic with DNA from 25 other species. In general, the data group, the parvorder (Fig. 2). This hypothe on 24000 hybridizations used for constructing the sis suggested an autochthonous adaptive radiation of phylogeny of all birds were obtained. The authors the oscines within , as well as the fact that argued that the true phylogeny can only be established some lineages of birds of the New and Old World, such through DNA hybridization, where the degree of rela as crows (Corvus), jays (, Gymnorhinus), and tionships is expressed through the temperature gradi (Campephagidae), have their roots in ent during hybridization. When constructing phyloge Australia rather than in the tropics of the Old and New netic schemes, the authors took the main provisions of World, where they currently have achieved great diver (Hennig, 1966), particularly the provisions sity. These views were supported by new data from fos that the rank of the category should be based on the sil finds and the reconstruction of paleobiotopes, time of its origin and that sister groups should be which pointed to a tropical rainforest in Australia at

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Moursebirds Coliiformes Coliae 24.5 Cuckoos Cuculiformes Cuculimorphae 23.7 Parrots Psittaciformes Psittacimorphae 23.1 Swifts 21.3 Hummingbirds Trochiliformes Apodimorphae 21.9 Turacos Musophagiformes Strigimorphae Passerae 20.4 Ouls Strigiformes 22.5 Pigeons Columbiformes 20.8 Cranes Gruiformes 20.1 , Ciconiiformes Passerimorphae Passerines 21.6 Passeriformes

Fig. 1. Composition of parvclass Passerae according to DNA hybridization data (from Sibley and Ahlquist, 1990).

Acanthisittidae Pittidae Furnariidae TYRANNI Conopophagidae Rhinocryptidae Thamnophilidae Tyrannidae

Climacteridae PASSERI Menuridae MENUROIDEA Ptilonorhynchidae Maluridae Meliphagidae Pardalotidae Eopsaltriidae Irenidae

Orthonychidae Passerida Corvida Pomatostomidae Laniidae Vireonidae Corvidae Bombycillidae Cinclidae Muscicapidae Sturnidae Sittidae Certhiidae Paridae Hirundinidae Regulidae Pycnonotidae Zosteropidae Sylviidae Alaudidae Nectariniidae Paramythiidae PASSEROIDEA Passeridae Fringillidae

Fig. 2. Phylogenetic relationships of passerine families according to DNA hybridization data (Sibley and Ahlquist, 1990).

BIOLOGY BULLETIN REVIEWS Vol. 4 No. 2 2014 PHYLOGENY AND CLASSIFICATION OF PASSERINE BIRDS, PASSERIFORMES 147 that time as a place of rapid adaptive radiation was significantly different from the previous ones. (Edwards and Boles, 2002). The opinion on the “primitiveness” of lyrebirds, as Corvida included, first, the superfamily Corvoidea, well as broadbills and scrubbirds (Atrichornithidae), consisting of the family Corvidae, which also included has changed. It was recognized that suboscines con birds from the traditional families of birdsofpara sists of two monophyletic groups, those of the Old and dise, old world orioles (Oriolidae), (Dicru New Worlds. Suboscines of the Old World, the families ridae), paradise flycatchers (Terpsiphone), woodswal of (Pittidae) and broadbills, are concentrated in lows (), and (). and SouthEast and are poor in their spe Besides Corvidae, the superfamily Corvoidea included cies composition, despite the high degree of morpho families of (Vireonidae), shrikes (Laniidae), Aus logical differences. In contrast, the adaptive radiation traloPapuan babblers (Pomatostomatidae), logrunners of suboscines of the New World is very extensive (about (), (Irenidae), and Australa 1100 species, mostly endemic to ), and sian robins (Eopsaltriidae). Second, Corvida included they are extremely diverse in morphology and behav the superfamily Meliphagoidea, consisting of the fam ior, being composed of the families of tyrant flycatch ilies of honeyeaters, (Maluridae), and ers (Tyrannidae), antshrikes (Thamnophilidae), diamondbirds (Pardalotidae), as well the superfamily (Rhinocryptidae), (Conopoph Menuroidea, consisting of the families of lyrebirds, agidae), ground (Formicariidae), and oven Australasian (Climacteridae), and bower birds (Furnariidae). birds (Ptilonorhynchidae). As a result of all the studies of passerines in the late Thus, the parvorder Corvida included birds that 20th century, the understanding of the phylogeny of were common in Australia and the New Guinea area, the order has greatly improved. The morphological and several of these families included species con cladistic analysis and DNA hybridization studies have verged to species from the families of another par generally given a quite similar pattern of branching of vorder, Passerida, from the Old and New World. the main divisions of the tree of passerines. The linear The parvorder Passerida, by Sibley and Ahlquist classifications of previous taxonomists have been (1990), includes three very large superfamilies—Pas replaced by hierarchical classifications based on the seroidea, Sylvioidea, and Muscicapoidea (Fig. 2). The concept of phylogeny (Raikow, 1987; Sibley and Ahl superfamily Passeroidea consists of the families of pas quist, 1990; Sibley and Monroe, 1990; Raikow and serines (Passeridae), true finches, painted berrypeck Bledsoe, 2000). ers (Paramythiidae), berrypeckers (Melanochariti dae), sunbirds, and larks. Here we must emphasize that into the family of passerines, besides the subfam PHYLOGENY ily of sparrows (Passerinae), Sibley and Ahlquist AND EVOLUTION OF PASSERINES placed weavers (Ploceinae) and estrildid finches ACCORDING TO DNA SEQUENCING DATA (Estrildinae), as well as the subfamilies of and Despite the great success of the studies set forth by (Motacillinae) and (Prunellinae). The Sibley and Ahlquist (1990), it soon began to be criti superfamily Sylvioidea, to the surprise of ornitholo cized with respect to various aspects of the phylogeny gists, consists, according to Sibley and Ahlquist, not proposed (Cracraft, 1992; Edwards and Boles, 2002; only of the families of Old World warblers, whiteeyes Ericson and Johansson, 2003; Barker et al., 2004). (Zosteropidae), (Cisticolidae), and gold However, the phylogeny and classification by Sibley crests (Regulidae), but also of (Pycnonotidae), and Ahlquist of passerine birds with 42 families swallows, longtail tits (Aegithalidae), tits, treecreepers became the basis for subsequent analyzes. In 2002– (Certhiidae), and (Sittidae), and the 2005, articles on the results of studies on nuclear DNA treecreepers also include wrens and sequencing of passerines were published (Barker et al., (). And in the superfamily Muscicapoidea, in 2002; Ericson et al., 2002, 2003; Ericson and Johans addition to the family of Old World flycatchers, Sibley son, 2003; Chesser, 2004; Beresford et al., 2005). and Ahlquist also included dippers, These works clearly confirmed the division of all Pas (Sturnidae), and (Bombycillidae). seriformes into two monophyletic —suboscines Thus, in the new classification based on the data of and oscines. Second,and most importantly, it was DNA hybridization (Sibley and Ahlquist, 1990), pas found that a family of small, socalled serines underwent a very large revision, both at the “wrens,” Acanthisittidae (or Xenicidae), having only level of families and at higher levels. By their mono four species, is nothing more than a sister group of all graph, these authors have provided more information other passerines. This family of birds has long been a for ornithologists to discuss and debate than any other taxonomic riddle and ornithologists have been inter bird taxonomists of the 20th century. DNA hybridiza ested in their obscure state and specific morphological tion studies, along with morphological analyses of the traits. In these birds, the syrinx has no specific features same time (Raikow, 1987; Prum, 1993), indepen inherent to the syrinx of oscines, and at the same time, dently gave quite a similar pattern of branching of the the bone of the middle ear has no bulbar shape, which main divisions of the tree of passerines, where this pat is typical for all suboscines (Feduccia, 1975). Sibley

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Suboscines Oscines

Corvida

Pittidae Philepittidae Meliphagoidea Passerida Tyranni Eurylaimidae Menuroidea Corvoidea Acanthisittidae

America Africa, Africa, Madagascar Australia Australia Australia, New Zealand Asia Asia the whole world

West East Gondwana

Gondwana

Fig. 3. Cladogramm of major groups of passerines according to nuclear DNA sequencing, their present distribution and suggested origin from Gondwana (Ericson et al., 2002). and Ahlquist (1990) placed them among the base of “treecreepers,” and “ robins” are recent derivatives of suboscines, assuming this by the molecular clock, and the corresponding groups in and America. Raikow (1987) identified them as a sister group of the The first doubts began to come in from paleontolo oscines, relying on the morphology of one of the leg gists. The assumption about the origin of passerines in muscles that appear in oscines as atavistic anomaly. the Southern Hemisphere has long been suggested Later, in the next paper of Barker et al. (2004), (Feduccia and Olson, 1982). Prior to the Middle based on the sequencing of the two singlecopy , a very small number of songbirds were nuclear genes from 144 passerine species from 45 fam found, and the earliest finds were dated to the Upper ilies, phylogenetic analysis confirmed the findings of of France. From this it followed that song previous studies on DNA sequencing (Barker et al., birds originated in the Southern Hemisphere, and 2002; Ericson et al., 2002) and found significant dis then spread to the north (Olson, 1988). However, crepancies with the branching of the tree of passerines there was not enough evidence to test this hypothesis, according to the data of DNA hybridization (Sibley until two small bones in the Early sediments in and Ahlquist, 1990). This led Barker et al. (2004) to the southeast Queensland, Australia were found assume that the phylogeny by Sibley and Ahlquist, as (Boles, 1995). These findings pushed back the age of well as the taxonomy that was partly based on it (Sibley passerine birds by almost 25 million years, to the time and Monroe, 1990), is highly problematic. All new when Australia had already begun to separate from studies recognized the impossibility of supporting the eastern Antarctica. hypothesis of Sibley and Ahlquist (1990) on the paral The phylogenetic relationships within Passerida, lel diversification of the northern, AfroEurasian Passer according to the new data (Ericson and Johansson, ida, and southern, AustralianNew Guinean Corvida, 2003; Ericson et al., 2003; Barker et al., 2004; Beres and their relationship as sister groups. According to the ford et al., 2005), also demanded a revision. There new data (Barker et al., 2004), Passerida is part of a para were doubts in the position of waxwings at the base of phyletic group Corvida, indicating that songbirds had Muscicapoidea, as well as in the whole group of originated not in the north, in Eurasia, but in Australia Sylvioidea, in particular, the phylogenetic relation and New Guinea as part of East Gondwana (Fig. 3). ships of and the clades composed of Up to 1970s–1980s, ornithologists believed that treecreepers, wrens, and nuthatches. Monophyly of various Australian and New Guinean “wrens,” the Old World family also was not supported.

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? Passerida

15 MYA or earlier 3–5 MYA ‘Corvida’ 3–5 MYA ‘Corvida’ Up to Suboscines of 80 MYA the New World Suboscines of 34MYA 82–85 MYA Up to 40 MYA the Old World Oscines

New Zealand “wrens”

Gondwana Fig. 4. Suggested dispersal routes of major passerine groups from Gondwana based on the data of phylogenetic relationships and biogeography (Ericson et al., 2002). MYA stands for “millions years ago.”

In the study of the phylogeny of the songbirds using But this is not consistent with the separation time of nuclear DNA sequencing (Treplin et al., 2008) based the continents, that is, earlier than 90 million years on a new molecular marker ZENK, along with three ago. Another version (Ericson et al., 2003) seems more conventional RAG1, RAG2, and cmyc, some new probable; the Kerguelen Plateau (now underwater in the data were obtained. This analysis was carried out with ) separated from Antarctica in the Late the clear support of the dividing the group Passerida , and suboscines of the Old World could (in the sense of Sibley and Ahlquist, 1990) into three spread to Africa and Asia over this plateau (Fig. 4). superfamilies, of which Sylvioidea is a sister for Although most of the previous systematic works on Muscicapoidea and Passeroidea. It was confirmed that suboscines were based on morphological traits, the Sylvioidea are not monophyletic. It was strongly sup work on DNA hybridization (Sibley and Ahlquist, ported that the family of tits should be separated from 1990) presented a scheme of their phylogeny that all other Sylvioidea, just as was previously expected coincided with traditional by several provisions. How (Alström et al., 2006). The position of larks remained ever, according to these data, the traditional families of unclear; there is evidence that they form a sister taxon tyrant flycatchers and ground antbirds were polyphyl to all other Sylvioidea, but according to another anal etic, which in regard to the latter family was supported ysis they form a monophyletic group with swallows. by the DNA sequencing data (Irestedt et al., 2002). The position of a number of genera and species in the The detailed phylogenetic relationships among subos family (sensu Alström et al., 2006) is cines of the New World were studied (Chesser, 2004) equally contradictory. The Common Grasshopper War on the basis of sequencing data of both the nuclear and bler (Locustella naevia) forms a monophyletic group with mitochondrial DNA in a sample of 53 taxa, of which genera and , but according to 44 are suboscines of the New World, three are subos other sources, it is a sister taxon of Sylvioidea. Also cines of the Old World, four are oscines, and one spe it is still at issue whether Acrocephalus and Hippolais are cies is the New Zealand (Acanthisitta chlo monophyletic (Helbig and Seibold, 1999). ris), and one species of (Campethera The monophyly of suboscines of both the Old and nivosa) as an outgroup. The results of the analysis con the New World suggests that these groups of birds were firmed that New Zealand wrens are indeed a sister divided a long time ago, and there are two versions of group to all other passerines, which coincides with the the circumstances of such a separation. One is based findings of previous studies (Barker et al., 2002; Eric on the hypothesis that suboscines were widespread son et al., 2002). Second, suboscines and oscines make before the separation of Africa and South America, up two distinct monophyletic groups. As for subos and that they divided when the continents separated. cines of the New World, one of its representatives, the

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Broadbilled ( aenigma), a resident based on a study of 32000 heterocyclic bases of aligned of rainforests from Panama to Ecuador, suddenly sequences of the nuclear DNA from 19 independent appeared to be suboscines of the Old World. If one genes in 169 species representing all the major groups excludes this species from the analysis, the monophyly of birds. This work gave a completely new picture of of the remaining suboscines of the New World is phylogenetic relationships. This system significantly clearly supported by all the molecular data. The differs from previous classifications based on research monophyly of the clades of and tyrant of the morphology and DNA hybridization and previ catchers is confirmed among them, although the ous studies of DNA sequencing, both nuclear and monophyly of tyrant flycatchers can be maintained mitochondrial. Nonmonophyly of a series of a tradi only if the subfamily Tityrinae is excluded from this tionally taken number of orders of birds was shown. family. As for the family of ground antbirds, it really For example, Apodiformes appeared as part of the turned to be polyphyletic. The genus Melanopareia radiation of nightjars, woodpeckers became part of and the (Oxyruncus cristatus) remained of Coraciiformes, and (Podicipediformes) turned unclear relationship. out to be closelyrelated to (Phoenicopteri The family, which is more than formes). Diurnal birds of prey (), tradi one third of all species of suboscines of the New World tionally consisting of () and Accip (about 400 species in 100 genera), was phylogeneti itrides? (), were included in different cally studied based on sequencing DNA from three branches of the tree of birds. The previously alleged nuclear introns of 128 taxa (Ohlson et al., 2008). The relationships between the New World vultures results confirmed a lot in the field of kinship relations (Cathartidae) and Ciconiiformes were not confirmed. in the family. In particular, a group of tityres indeed As for passerine birds, Hackett et al. (2008) confirmed makes up a separate family Tytyridae, and some genera the inviolability of dividing them into oscines and subos of tyrant flycatchers, such as the cines, as well as a special base position of the New (Onychorhynchus), the Ruddytailed Flycatcher (Tere Zealand wrens with respect to all Passeriformes. It was notriccus), and (Myiobius), which are usually shown that passerines are included in the biggest clade— referred to tyrant flycatchers, should be derived from the clade of ground birds, also consisting of woodpeckers, this family and perhaps may be related to tityres. The diurnal raptors, owls, rollers, parrots, , and very family Tyrannidae consists of two main lineages. . Most unexpected in this case are the relation One of them is the clade of the subfamily Pipromor ships of sister groups between passerines and parrots and phinae (flatbilled tyrant flycatchers, , antpipits, a sister relation of this clade to the clade of falcons. At the , and spectacled bristle tyrants). The sec same time, accipitrides are quite distanced from them, ond clade is divided into two subclades, one consists of being close to the owls (Fig. 5). Elaeniinae (, tyrants, , etc.), Another recent significant publication (Pacheco and the second of the three groups—Myiarchinae et al., 2011) reports on a new analysis of the time of (genus , etc.), Tyranninae (tyrant pirate, origin and evolutionary relationships among the etc.), and Fluvicolinae (genus , etc.). orders of modern birds based on the use of complete Attempting to reconstruct the of the ancestors mitochondrial genomes, which, as the authors say, are of these birds and an estimation of the time of diver the main sources of data for studies of the evolution of gence suggests that the basic events of divergence of birds. This paper, based on 80 complete genomes, of Tyrannidae took place in the wet forest during the Oli which 17 are new in such studies, analyzes many taxa gocene. Largescale diversification in open habitats was of modern birds from the Old and New Worlds. inherent to birds from the groups Elaeniinae, Myiarchi Although the discussed paper showed moderate con nae, Tyranninae, and Fluvicolinae since the mid sistency of the results of molecular studies with a num Miocene, that is, about 15 million years ago. ber of traditional views (Payevsky, 2012), many of One of the genera of tyrant flycatchers, black these results occurred to be as new as the data of Hack tyrants (), was provided with the first ett et al. (2008). It has shown a common origin of molecular phylogenetic hypothesis based on the nightjars, swifts, and cuckoos, as well as the face that sequencing of the nuclear and mitochondrial DNA Columbiformes and are monophyl (Hosner and Moyle, 2012). The analysis determined etic and are sister groups. Passerines in this work, as in monophyly of the genus, with its most likely sister all the previous studies, are recognized as a monophyl group of the genus . The genus Knipolegus etic group together with suboscines and oscines as two forms three clades: the first is of three species limited separate clades, together with New Zealand wrens as a in spread by the northern part of South America; the sister group. However, the suggested relation of passe second is again of three species found in southeastern rines and parrots as sister groups and falcons as a Brazil; and the third clade is formed of six species closely related group (Hackett et al., 2008) was not widespread in the southern part of South America. confirmed by this analysis. Instead, a clade with Of the further works on bird DNA sequencing, two branching into parrots and owls was found, which had are the most remarkable. The first is the publication by a common ancestor with passerines, rollers, wood Hackett with 17 coauthors (Hackett et al., 2008), peckers, and trogons (Fig. 6).

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Oscines Suboscines Parrots Falcons and todies Rollers and eaters Picidae and Trogons Mousebirds Owls Accipitridae Scolopacidae and guillemots and stone

Fig. 5. Part of of birds according to nuclear sequencing data. Simplified scheme of cladogram (Hackett et al., 2008).

Lined Forest Falcons Falconidae American Kestrel Osprey Goshawk Accipitridae Accipitridae Mountain HawkEagle Blyth’s HawkEagle Barn Owls Strigiformes Cobaltwinged Parakeet BrownThroated Parakeet Duskybilled Parrotlet Peachfaced Parrots Psittaciformes Sacred Dollarbird Wrinkled Kingfishers, Hornbills Coraciiformes Silverycheeked Hornbill Southern Ivorybilled Pileated Woodpecker Woodpeckers Piciformes Whitetailed Trogons Trogoniformes Zebra Steel Weaver Passerines Blackcap Passeriformes Lyrebird Greyheaded Broadbill

Fig. 6. Phylogenetic relationships among seven orders of birds according to data of sequencing complete mitochondrial genomes (Pacheco et al., 2011).

PHYLOGENY OF FLYCATCHER ing, may be of interest (Zuccon and Ericson, 2010; COMPLEX (MUSCICAPIDAE Sangster et al., 2010). Until recently, according to the sensu DICKINSON, 2003) traditional view of taxonomists (for example, Wet From molecular studies on phylogeny of individual more, 1960; Kartashev, 1974), chats with groups of passerines at the family level, two works on were attributed to thrushes, and Old World flycatchers studying the complex chats–flycatchers (when the were isolated into the family Muscicapidae. It has long group of chats also includes wheatears), based on a been known that chats, wheatears, and flycatchers combination of nuclear and mitochondrial sequenc have morphological and behavioral similarities. The

BIOLOGY BULLETIN REVIEWS Vol. 4 No. 2 2014 152 PAYEVSKY genus (subfamily Muscicapinae) was usu The genus Erithacus turned out to be a part of the ally considered close to thrushes. According to the group of African “robinlike” birds (Stiphrornis, taxonomy of Mayr and Amadon (1951), the volume of , Pseudalethe, Cichladusa, Pogonocichla, and the family was the largest since at Sheppardia), and the genera , , and the rank of subfamilies. Besides flycatchers, it Enicurus belong to the large Asian clade. The clade of included thrushes, babblers, Old World warblers, king (, Chaimarornis, and Rhyacornis) lets, wrens, dippers, and . In the list of is in the base of a group of genera together with Mon birds of the world (Dickinson, 2003), the family Mus ticola, , Oenanthe, Cercomela, and others cicapidae includes chats, wheatears, flycatchers, rob (Zuccon and Ericson, 2010). According to the data of ins (Erithacus), nightingales (Luscinia), redstarts another analysis (Sangster et al., 2010), the position of (Phoenicurus) and many other taxa (in total, 275 spe the (Erithacus rubecula) in the clade cies in 48 genera). Species of this family are widely dis of African species and sisterly relations among tributed in different regions of the world, living in a and Monticola, Phoenicurus, Saxicola, and variety of habitats. Oenanthe were clearly confirmed. The proximity of thrushes and Old World flycatch ers was mostly based on two synapomorphies—fea PROBLEM OF PHYLOGENY OF “NEW WORLD tures of the syrinx morphology and mottled NINEPRIMARIED OSCINES” of young birds. Some studies of the subfamilies Turdi nae and Muscicapinae considered them as sister Since the 19th century, the number of primary groups (Sibley and Ahlquist, 1990; Barker et al., 2004; of passerine birds has been seen as a taxo Johansson et al., 2008), although other studies (Zuc nomic trait, and one group of birds was called “passe con et al., 2006; Voelker and Spellman, 2004) did not rines with nine primaries,” in contrast to passerines suggest close relationships between them, and at the with ten primaries of varying degrees of development. same time the views that Old World flycatchers and Links have been found between the number of prima chats make up one monophyletic branch were con ries and other traits; for example, it was believed that firmed. According to some molecular studies (Cibois in passerines with ten welldeveloped primaries the and Cracraft, 2004; Voelker and Spellman, 2004), a vocal apparatus is of imperfect development (Wallace, 1874). The group of birds with nine primaries initially typical Old World flycatcher of the genus Ficedula and included the families Hirundinidae, , the rock Monticola belong to the subfamily of Bombycillidae, Dicaeidae, Mniotiltidae (now Paruli stonechats Saxicolinae, while shamas Copsychus—to dae), Coerebidae, Drepanididae, Tanagridae (now Old World flycatchers. Thraupidae), Icteridae, and Fringillidae. Of these To analyze the phylogenetic relationships using the families, at present, the group of the “New World data of nuclear and mitochondrial sequencing in the nineprimaried oscines,” also called the “Fringillidae chatflycatcher complex (Zuccon and Ericson, 2010), clade” (Sibley and Ahlquist, 1990), include Parulidae, 46 species were selected from Saxicolinae and 20 spe Coerebidae, Drepanididae, Thraupidae, Icteridae, cies from flycatchers, as well as six species of thrushes Fringillidae, and the American sparrows from Emberi as an outgroup, representing the main lines of Turdi zidae, and had sometimes included Vireonidae, since dae; the analysis was carried out using Bayesian prob the latter may have both nine and ten primaries. At the ability and maximum likelihood criterion. The results same time, despite the widespread use of this term to showed that the commonly accepted separation of this day, many authors point out that in fact all of these ground feeding stonechats and wheatears and air birds have 10 primaries, but that the 10th one (or first, feeding flycatchers does not reflect the existence of if one counts the primaries not centrifugally but cen monophyletic groups. Morphological adaptations for tripetally) is reduced, sometimes to a very large extent. air feeding (broad , perioral bristles, short tar The most comprehensive and detailed study of the sometatarsus) and the typical behavior of flycatchers problem of one rudimentary out of ten prima apparently evolved independently in the three line ries was carried out by Stegmann (1962), who showed ages. Always believed to be thrushes, the genera of there are actually always ten primaries, but one of whistling thrushes (Myiophonus), shortwings (Bra them can be of very different lengths. The same con chypteryx), and alethes () turned out to belong to clusion was reached by Hall (2005) on the basis of a the family of Old World flycatchers, and their morpho special study of 104 species of birds. She proved that, logical and ecological similarity with true thrushes, while being extremely rudimentary, the 10th primary apparently, is the result of convergence. One of the (or first, by centripetal counting) is hidden under the main lineages includes three clades—Alethe, the clade covert feather of the previous (or subsequent) flight of African flycatchers (Sigelus, , Melaenor feather; only when lifting the latter one can see it. nis, Fraseria, Empidornis, and Bradornis) and birds of Sibley and Ahlquist (1990) assumed the mono the genus Muscicapa, and finally the clade of the gen phyly of the socalled New World nineprimaried era Erythropygia, Cercotrichas, Copsychus, Saxico oscines according to the data of DNA hybridization. loides, and Trichixos. The DNA sequencing analysis generally supports this

BIOLOGY BULLETIN REVIEWS Vol. 4 No. 2 2014 PHYLOGENY AND CLASSIFICATION OF PASSERINE BIRDS, PASSERIFORMES 153 monophyly if they are not added with the family of sizes and different regional habitats are presented in true finches (Ericson et al., 2003), but in terms of the two papers by Ricklefs (2003, 2006) on global variation relationships within the group there is no agreement. in the diversification rate of passerines. The existence The most clearly supported opinion based on both of significant variations in the level of species diversity nuclear and mitochondrial genes states that Icteridae of different clades of birds led to the idea that activa and Parulidae are sister groups. Surprisingly, accord tion of the diversification rate occurs at certain key ing to the molecular data, the genera Calcarius (Lap innovations, such as promiscuity, plumage dichroma land ) and (Snow ) are tism, and other phenomena due to sexual selection. not included in the group of American buntings and However, the search for key innovations is very diffi are in a basal position to all other “nineprimaried cult because of the different ecology, lifestyle, and geo oscines.” Most likely, the ancestors of the latter arrived graphic distribution. The hypothesis of the existence in either from Asia via the Bering of a higher diversification rate in the tropical latitudes Strait or from via Greenland, and the Lapland due to high air temperatures and intense energy flow Longspur and are descendants of earlier has been repeatedly discussed (Allen et al., 2002; immigrants from the Old World (Ericson et al., 2003). Ricklefs, 2006, etc.). This hypothesis was tested by comparing sister taxa, as they are of the same age. However, the difficulty of selecting sister clades that DEMOGRAPHIC PARAMETERS have primary differences in the latitudinal distribution AND SPECIATION RATE did not permit latitudinal comparisons in the raw, An important issue in the construction of relation without the influence of other factors. To solve this ships consists in the relation of demographic factors problem, Ricklefs (2006) compared the rate of diversi and the DNA evolution rate. The assumption that the fication among clades in several taxa of passerine birds generation lifetime duration affects the rate of accu that were endemic to the tropics and the temperate mulation of mutations in the DNA, and hence the rate zone of America. As a result, it was found that the net of the genome evolution (Kohne et al., 1972), led to rate of diversification of passerine birds is significantly the logical conclusion that the shorter the generation higher in both the larger areas and the tropical regions. lifetime was, the higher the rate of molecular evolution At the same time, the rates of diversification decrease would be. Initially, a singlecopy DNA comparison in with the age of clades, and this suggests that the filling longlived and shortlived birds (in the example of of the ecological space limits further diversification. ) did not confirm this finding (Sibley In connection with the above data, the question and Ahlquist, 1983), but later it was found to be erro arises of the existence of differences in the level of neous (Sibley and Ahlquist, 1990). In birds with divergence between species. The assessment of the delayed sexual maturity and a long generation lifetime, degree of genetic differentiation between populations the DNA evolution rate is slower than in birds that and species in terms of the share of structural genes in begin to breed at an early age and have a short genera the compared taxa is implemented in the index of tion lifetime. The latter include the vast majority of genetic distance. The comparison of genetic distances passerines (as well as , , some between species showed that in birds they are minimal waterfowl) that begin to breed at the age of one in relation to the genetic distances in other species of (Ricklefs, 1972; Payevsky, 1985). Therefore, the : three times less than in mammals, five times increased rate of their evolution can be explained by less than that of reptiles, and more than ten times less peculiarities of their demographics. Anyway, these than that of amphibia (Borkin and Litvinchuk, 2010). species had similar rates of changes in the genome, It is still unknown whether these differences are asso which has been shown by branches that are longer or ciated with the speciation rate. of the same in length in the dendrograms when com pared to the groups with very different lifetimes of gen erations. In some cases, when a species starts to breed CONCLUSION at the age of less than one year, such as estrildid This review shows that the extraordinarily rapid finches, the branches are longer than those branches development of contemporary molecular research of their closely related forms with reproduction at a aimed at the study of the systematics of birds leads to later age (Sibley and Ahlquist, 1990). results that from the standpoint of traditional views The optimum values of species diversity are depen often seem strange, unexpected, and sometimes erro dent on the degree of stability of the environment, neous (Cracraft, 1992; Balatskii, 1997; Koblik, 2001). where this degree is expressed in the intensity of As E.A. Koblik rightly pointed out (2001), it comes to resource flows; when they increase, these values the absurd situation where representatives of genera increase as well. Thus, resources are used more effi that are known to be close in terms of a complex of ciently because of the differentiation of ecological traits are assigned to different families. The paradox of niches (Bukvareva and Aleshchenko, 2010). The the situation is aggravated by the fact that each new extensive material and discussion of differences in this molecular study of phylogenetic relationships of birds respect among the clades of passerines of different of both higher taxa and others largely rejects findings

BIOLOGY BULLETIN REVIEWS Vol. 4 No. 2 2014 154 PAYEVSKY of previous authors and promotes new perspectives on Barraclough, T.G., Harvey, P.H., and Nee, S., Sexual selec the basis of their results. Numerous examples of sys tion and taxonomic diversity in passerine birds, Proc. R. tematic innovations in the order of passerine birds, Soc. B, 1995, vol. 259, pp. 211–215. discussed above, clearly demonstrate this. Beresford, P., Barker, F.K., Ryan, P.G., and Crowe, T.M., African endemics span the tree of songbirds (Passeri): Can one expect real progress, accepted by a major molecular systematics of several evolutionary ‘enig ity of taxonomists, in this area? Presumably, only an mas’, Proc. R. Soc. B, 2005, vol. 272, pp. 849–858. integrated approach, with the use of different molecu Boles, W.E., The world’s oldest , Nature, 1995, lar studies and conventional comparative morpholog vol. 374, pp. 21–22. ical analysis, may lead to such progress. With varying Borkin, L.Ya. and Litvinchuk, S.N., Species and speciation degrees of certainty, this is demonstrated by those pro in animals: molecular and genetic assessment (genetic visions that exist today in the phylogeny of higher taxa distances), in Tr. Mezhd. konf. “Charl’z Darvin i sovre of passerine birds. Some of them are “unshakable,” mennaya biologiya” (Trans. Int. Conf. “Charles Darwin supported by both morphological and different molec and Modern Biology”), St. Petersburg: ular data: (1) the division into two suborders, Oscines Istoriya, 2010, pp. 236–250. and Suboscines; (2) the special systematic position of Bukvareva, E.N. and Aleshchenko, G.M., Optimization of New Zealand wrens; and (3) the division of Subos diversity of superorganism systems as a mechanism for cines into groups of birds of the New and Old Worlds. their development on ecological, microevolutionary Other provisions are probable, supported by some and evolutionary scales, Usp. Sovrem. Biol., 2010, morphological and some molecular data, for example, vol. 130, no. 2, pp. 115–129. the close relationships among the groups of wood Cardillo, M., Latitude and rates of diversification in birds peckers, rollers, and trogons. And, finally, there are the and butterflies, Proc. R. Soc. B, 1999, vol. 266, controversial provisions, supported only by some pp. 1221–1226. molecular data: (1) the diversion of the clade of passe Chesser, R.T., Molecular systematics of New World subos rines from the clade containing cranes and storks, (2) cine birds, Mol. Phylogenet. Evol., 2004, vol. 32, the relations of sister groups between passerines and pp. 11–24. parrots, and (3) the proximity of passerines to falcons. Cibois, A. and Cracraft, J., Assessing the passerine “Tapes try”: phylogenetic relationships of the Muscicapoidea In conclusion, we can express cautious optimism inferred from nuclear DNA sequences, Mol. 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