Phylogenetic relationships within Passerida (Aves: Passeriformes): A review and a new molecular phylogeny based on three nuclear intron markers

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Abstract

The avian clade Passerida was first identified based on DNA–DNA hybridization data [C.G. Sibley, J.E. Ahlquist, Phylogeny and Classification of Birds, 1990, Yale University Press, New Haven, CT]. Monophyly of the Passerida, with the exception of a few taxa, has later been corroborated in several studies; however, the basal phylogenetic relationships have remained poorly understood. In this paper, we review the current knowledge of the phylogenetic relationships within Passerida and present a new phylogeny based on three nuclear introns (myoglobin intron 2, ornithine decarboxylase introns 6 and 7, as well as β-fibrinogen intron 5). Our findings corroborate recent molecular hypotheses, but also identify several hitherto unrecognized relationships.

Introduction

Of the world’s approximately 9600 species of birds, nearly 60% belong to the passerine clade, Passeriformes (Sibley and Monroe, 1990). Compared with other avian groups of comparative age (cf Ericson et al., 2006), no other clade has evolved such great species richness and range of ecological diversification as the passerines. The group is represented in nearly all non-marine habitats and is distributed on all of the continents except Antarctica. In addition, passerines exploit a wide range of food resources, and within this clade many groups have developed morphological specializations for varied diets, including insectivory, (e.g. warblers), nectarivory (e.g. sunbirds), frugivory (e.g. cotingas), granivory (e.g. finches), carnivory (e.g. shrikes), or herbivory (plantcutters), as well as different feeding strategies (e.g. aerial hunting, bark or foliage gleaning and sallying). Most of the anatomical variation within the passerines relates to these differences in foraging and as a result earlier classifications and phylogenetic hypotheses based on morphology do, to a large extent, reflect such functional groups (e.g. Beecher, 1953). Recent molecular-based studies (e.g. Barker et al., 2004, Beresford et al., 2005, Fuchs et al., 2006, Sibley and Ahlquist, 1990); however, suggest that many of these traditional groups are polyphyletic, and that morphologically similar ecotypes have evolved independently in different parts of the world (Sibley and Ahlquist, 1990).

The first comprehensive molecular study, based on DNA–DNA hybridization data by Charles Sibley and co-workers (summarized in Sibley and Ahlquist, 1990, Sibley and Monroe, 1990) suggested a strikingly different view of the phylogenetic relationships of birds compared to previous phylogenetic hypotheses and classifications based on morphological data; in particular within the passerine birds. However, the DNA–DNA hybridization study met with severe criticism (e.g. Harshman, 1994, Houde, 1987, Mindell, 1992, Sarich et al., 1989) and several relationships suggested by Sibley and Ahlquist (1990) have later been shown to be erroneous (e.g. Barker et al., 2004, Ericson et al., 2002a, Johansson and Ericson, 2003). Nevertheless, the results of Sibley and Ahlquist (1990) have served as the framework for many ecological and comparative phylogenetic studies (e.g. Bennett and Owens, 2002, Fjeldså, 1994, Hawkins et al., 2006, Starck and Ricklefs, 1998). Today, studies based on DNA sequencing have begun to converge on a new passerine topology, which includes features from the DNA–DNA hybridization dendrogram of Sibley and Ahlquist (1990) and traditional classification in addition to several novel relationships. Unfortunately, many areas of conflict and uncertainty remain in the passerine tree, and there is a clear need to increase the number of independent loci sequenced, as well as the extent of taxon sampling in order to help resolve difficult nodes.

In this paper, we review recent hypotheses of phylogenetic relationships within in one of the largest clades of passerine birds, the Passerida. In particular, we aim to identify parts of the phylogenetic tree that appear to be robust as well as those parts that remain uncertain. We also present a phylogeny of the Passerida based on data from three nuclear markers (myoglobin intron 2, ornithine decarboxylase (ODC) introns 6 and 7, as well as β-fibrinogen intron 5), in total ∼2.3 kb for 90 species. Our primary objective was to examine the basal relationships within Passerida with an emphasis on the early divergences within Sylvioidea, and investigate the phylogenetic position of several taxa of uncertain phylogenetic affinities. In addition, we constructed a phylogeny based on as a six-gene dataset (7388 base pairs) for a subset of these taxa in order to examine the effect of increased character sampling on the topology.

The monophyly of Passeriformes is strongly supported by morphological (Raikow, 1982) as well as molecular data (Cracraft et al., 2004, Johansson et al., 2001), as is the traditional division of the passerines into two major clades, the Oscines and Suboscines. This latter subdivision was based initially on syringeal morphology (Ames, 1971, Müller, 1878), but has also been recovered in several molecular studies (e.g. Ericson et al., 2002a, Irestedt et al., 2001, Lovette and Bermingham, 2000). In addition to these two traditional groups, recent molecular findings (Barker et al., 2002, Barker et al., 2004, Ericson et al., 2002a) suggest that two species endemic to New Zealand, the Rifleman (Acanthisitta chloris) and the Rock Wren (Xenicus gilviventris) (Acanthisittidae) constitute the sister-group to all other passerines. This finding has had great implications for the understanding of the biogeographic origin of passerine birds (Barker et al., 2004, Edwards and Boles, 2002, Ericson et al., 2003).

Of these three groups, oscines are the most numerous with more than 4500 species. Although the oscines have an almost worldwide distribution, the basal lineages of oscines are primarily distributed in the Australasian region, suggesting that the clade originated within this region (Barker et al., 2002, Barker et al., 2004, Ericson et al., 2002a, Jønsson and Fjeldså, 2006a). Among the several oscine lineages that have spread to other parts of the world, Passerida, with approximately 3500 species, is the largest. This clade was first recognized from DNA–DNA hybridization data (see Sibley and Ahlquist, 1990), and its monophyly has later been supported by analyses of DNA sequence data (Barker et al., 2002, Barker et al., 2004, Ericson et al., 2002a, Ericson et al., 2002b), as well as by an unique insertion of one codon in the c-myc gene (Ericson et al., 2000).

Although the general concept of a monophyletic Passerida has been supported by several studies, not all species and clades included in the Passerida by Sibley and Monroe (1990) have been confirmed to be part of this clade (Table 1, Table 2). For instance, DNA sequences from the genes RAG-1 and RAG-2 (Barker et al., 2004) suggest that the New Guinean Crested Berrypecker (Paramythia montium—Paramythiidae) as well as the berrypeckers and longbills (Toxorhamphus, Oedistoma, Melanocharis—Melanocharitidae), both placed in the Passerida by Sibley and Monroe (1990), instead form part of two other Oscine clades, the “core Corvoidea” (sensu Barker et al., 2004) and the cnemophiline birds-of paradise, respectively. Further, some species from Madagascar, for example the four Newtonia species (Newtonia) and Crossley’s Babbler (Mystacornis crossleyi), also appear to be part of the “core Corvoidea” (Cibois et al., 1999, Cibois et al., 2001, Yamagishi et al., 2001) rather than members of the Passerida radiation.

DNA sequence-based studies have also indicated that several of the taxa that were not included in Passerida by Sibley and Monroe (1990) may in fact be part of this radiation (Table 2). For example, the fairy-bluebirds (Irena), leafbirds, (Chloropsis), canary-flycatchers (Culicicapa) and several species traditionally placed among the monarchine flycatchers (Erythrocercus and Elminia, including E. nigromitrata, and E. albonotata) are nested within Passerida (Barker et al., 2004, Pasquet et al., 2002). The Tibetan Ground-Jay (Pseudopodoces humilis), which in all previous classifications were placed among the crows (Corvini sensu Sibley and Monroe, 1990), has recently been shown to be a ground-living tit (Paridae) (James et al., 2003).

Sibley and Ahlquist (1990) recognized three clades within Passerida: Muscicapoidea, Sylvioidea, and Passeroidea, with Muscicapoidea basal relative to the other two clades. In the analyses of Sibley and Ahlquist (1990) these clades are; however, separated by very short internodes and subsequent DNA sequence-based studies have not been able to confirm their monophyly (Barker et al., 2002, Barker et al., 2004, Beresford et al., 2005, Ericson and Johansson, 2003, Fuchs et al., 2006). Indeed, if only the highly supported nodes in these molecular studies are considered, Passerida is divided into at least nine clades with uncertain relationships (Fig. 1).

Two of these clades have a taxonomic composition rather similar to Muscicapoidea and Passeroidea (sensu Sibley and Monroe, 1990). Muscicapoidea (sensu Sibley and Monroe, 1990) included dippers (Cinclidae), thrushes (Turdinae), Old World flycatchers and chats (Muscicapinae), starlings and oxpeckers (Sturnini), mimids (Mimini) as well as waxwings, silky-flycatchers and palmchats (Bombycillidae). Monophyly of a clade containing all these groups but Bombycillidae has been supported in several subsequent molecular studies (Barker et al., 2002, Barker et al., 2004, Cibois and Cracraft, 2004, Ericson and Johansson, 2003, Voelker and Spellman, 2004), although this clade appears to also include the three species of Philippine creepers (Rhabdornis) (Cibois and Cracraft, 2004, Lovette and Rubenstein, 2007, Zuccon et al., 2006). The placement of Bombycillidae with this group, as suggested by Sibley and Ahlquist (1990), has not been recovered with strong support in any subsequent study (Barker et al., 2002, Barker et al., 2004, Beresford et al., 2005, Cibois and Cracraft, 2004, Ericson and Johansson, 2003, Fuchs et al., 2006, Voelker and Spellman, 2004). Rather, several of these studies have indicated a more distant relationship, but neither of these alternative placements of the Bombycillidae are strongly supported, and the phylogenetic position of this clade must be considered unresolved within the Passerida. Hereafter we use the term Muscicapoidea for the clade containing: Cinclidae, Turdinae, Muscicapinae, Sturnini, Mimini, and exclude Bombycillidae from this group (Fig. 1).

With a few exceptions, Sibley and Monroe’s (1990) circumscription of Passeroidea (Fig. 1) has also been supported by subsequent studies based on DNA sequencing. The berrypeckers and longbills (Paramythiidae and Melanocharitidae), which were placed in Passeroidea by Sibley and Monroe (1990), seemingly are not part of this radiation but rather fall outside the Passerida (see above). The larks (Alaudidae) have also been shown to fall outside the Passeroidea clade, although still within the Passerida radiation (e.g. Barker et al., 2004, Ericson and Johansson, 2003, Sheldon and Gill, 1996). A few clades have also recently been suggested to be part of Passeroidea; for instance Barker et al. (2004) placed the fairy-bluebird (Irena) and leafbirds, (Chloropsis) as one of the most basal clades in Passeroidea and sister to the Nectariniidae. In addition, the Dapple-throat (Arcanator orostruthus) and Spot-throat (Modulatrix stictigula), previously placed among babblers (Timalini, Sibley and Monroe (1990), or with the bulbuls and thrushes, respectively (Rand and Deignan, 1960, Ripley, 1964), have now been suggested to have a basal position within the Passeroidea (Barker et al., 2004).

Circumscription of Sylvioidea, the third of the three primary Passerida clades of Sibley and Ahlquist (1990), is more uncertain. Recent DNA sequence-based studies (e.g. Alström et al., 2006, Barker et al., 2004, Ericson and Johansson, 2003, Fuchs et al., 2006) have not been able to confirm monophyly of the Sylvioidea sensu Sibley and Ahlquist (1990). In part, this appears to be a result of poor resolution and low statistical support for the indicated relationships, but could also indicate that some clades included in the Sylvioidea sensu Sibley and Ahlquist (1990), e.g. the titmice and penduline tits (Parinae and Remizinae, respectively), kinglets (Regulidae) and Hyliotas (Hyliota), represent deep, isolated lineages within Passerida.

Another group included in the Sylvioidea sensu Sibley and Ahlquist (1990), but whose affinity with that group needs further evaluation, includes the nuthatches (Sittinae), wallcreepers (Tichodrominae), creepers (Certhiini), wrens (Troglodytinae) and gnatcatchers (Polioptilinae) (e.g. Alström et al., 2006, Barker et al., 2004, Cracraft et al., 2004, Ericson and Johansson, 2003). This clade was also recovered by Sibley and Ahlquist (1990) based on DNA–DNA hybridization analyses but their data suggested that the Black-capped Donacobius (Donacobius atricapillus) and the Verdin (Auriparus flaviceps) also belong to this clade, although this has been challenged in recent sequence-based studies (Alström et al., 2006, Barker, 2004, Gill et al., 2005). In this paper, we refer to this clade (excluding Donacobius and Auriparus) as Certhioidea (following Cracraft et al., 2004) (Fig. 1).

Given the uncertainties in the phylogenetic placement of several of the clades included in Sylvioidea (sensu Sibley and Monroe, 1990), the term “Sylvioidea” has now become restricted to a much smaller group comprising the “families” (sensu Sibley and Monroe, 1990) Aegithalidae (long-tailed tits), Hirundinidae (swallows), Pycnonotidae (bulbuls), Cisticolidae (African warblers), Zosteropidae (white-eyes), Sylviidae (Old World warblers and babblers) and Alaudidae (larks) (Alström et al., 2006, Beresford et al., 2005, Ericson and Johansson, 2003). However, several studies have demonstrated that few of these “families”, as circumscribed by Sibley and Monroe (1990) are monophyletic (Alström et al., 2006, Beresford et al., 2005, Cibois, 2003, Cibois et al., 2001, Dickinson, 2003, Moyle and Marks, 2006, Nguembock et al., 2007, Sefc et al., 2003). The only exceptions are Hirundinidae and Alaudidae, whose monophyly are well supported by both morphological and molecular data (Mayr, 1958, Sheldon et al., 2005) and Zosteropidae, for which there is currently no molecular data available to confirm or refute the suggested monophyly of this lineage.

No group within Sylvioidea (sensu stricto) poses a greater taxonomic dilemma than the Sylviidae. Recent molecular studies have demonstrated that the various genera included in this “family” are scattered among the other Sylvioidea clades and several species in this group constitute previously unrecognized radiations rather distantly related to other sylvioid taxa. For example, Beresford et al. (2005) identified a clade, informally termed the “Sphenoeacus-group”, which includes among others the Cape Grassbird (Sphenoeacus afer), Crombecs (Sylvietta) and the Rockrunner (Achaetops pycnopygius) and suggested that this clade constitutes a relatively basal clade within Sylvioidea. Another recently identified clade with uncertain affinities within the Sylvioidea is the endemic Malagasy “warbler” radiation “Bernieridae” that includes approximately 10 species of sylvioid birds that in earlier classifications were considered to be part of different lineages such as bulbuls, babblers, and Old World warblers (Cibois et al., 1999, Cibois et al., 2001, Fjeldså et al., 1999). In addition, the Bearded Reedling (Panurus biarmicus), which has generally been placed with parrotbills, the Nicators (Nicator), previously considered to be bulbuls (Pycnonotidae) or bush-shrikes (Malaconotidae), and the Erythrocercus flycatchers, previously placed with monarchine flycatchers, all apparently constitute isolated branches with uncertain affinities within Sylvioidea (Beresford et al., 2005, Ericson and Johansson, 2003, Fuchs et al., 2006, Pasquet et al., 2002). Alström et al. (2006) proposed a new classification for Sylvioidea (sensu stricto) based on myoglobin and cytochrome b sequence data that incorporated some but not all of these changes and divided the traditional Sylviidae into six clades: Cettiidae, Phylloscopidae, Acrocephlidae, Megaluridae, Cisticolidae, and Timaliidae, in addition to the other sylvioid clades (Aegithalidae, Hirundinidae, Pycnonotidae, and Alaudidae).

In addition to Muscicapoidea, Passeroidea, Sylvioidea and the other comparably small Passerida clades (Fig. 1), molecular DNA data have identified yet another previously unrecognized clade within Passerida with uncertain phylogenetic affinities (Barker et al., 2004, Beresford et al., 2005, Pasquet et al., 2002). This clade, termed Stenostiridae, contains several species which were previously thought to be monarchine flycatchers and includes the Oriental canary-flycatchers (Culicicapa), the African blue-flycatchers (Elminia) including the crested-flycatchers E. nigromitrata and E. albonotatus (Pasquet et al., 2002), and the Fairy-flycatcher (Stenostira scita, Beresford et al., 2005).

Section snippets

Terminology

Scientific names of species follow Dickinson (2003), with the exception of Modulatrix orostruthus which we retain in Arcanator (see results). The names of higher-level clades follow Sibley and Monroe (1990) with the exceptions as noted in the introduction (see also Fig. 1).

Taxon sampling and outgroup selection

We sampled representatives of all major clades of Passerida (see Section 1), but aimed to include a broad range of taxa whose systematic position has been disputed in the literature. Our taxon sampling includes the hyliotas,

Sequence attributes

The concatenated alignment of the three-gene segments contain 2315 aligned positions: myoglobin 794 base pairs (bp), ODC 803 bp, excluding a 625 bp long insertion in Motacilla and Amaurocichla, and β-fibrinogen 718 bp. Of these, 1055 bp (318, 380, and 357 bp, respectively) are potentially parsimony informative. Base composition was biased in favor of Adenine and Thymine in all genes (myoglobin: A = 0.28, C = 0.22, G = 0.23, T = 0.26; ODC: A = 0.28, C = 0.17, G = 0.20, T = 0.35; fibrinogen: A = 0.30, C = 0.17, G = 0.21, T = 

Discussion

Although Passerida constitutes the dominant group of passerines in the northern hemisphere, the origin and early diversification of the oscine passerines in Australasia suggests that the now worldwide distributed Passerida originated from an ancestral species that dispersed from the Australasian region (Barker et al., 2002, Ericson et al., 2002a, Ericson et al., 2003, Fuchs et al., 2006), possibly in the Eocene (Barker et al., 2004). Two alternative routes for dispersal out of the Australasian

Acknowledgments

We are very grateful to the curators and collection managers at the Durban Museum, Field Museum of Natural History, Museum of Vertebrate Zoology at the University of California, Berkeley, Swedish Museum of Natural History, Percy FitzPatrick Institute at the University of Cape Town, and the Zoological Museum at the University of Copenhagen for kindly providing us with tissue and blood samples for this study. We also acknowledge the field collectors associated with these institutions for their

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