A multi-gene phylogeny reveals novel relationships for aberrant genera of Australo-Papuan core Corvoidea and polyphyly of the Pachycephalidae and Psophodidae (Aves: Passeriformes)

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Abstract

The core Corvoidea is the largest and most diverse oscine assemblage within the Australo-Papuan region. Although central to an understanding of the evolutionary history and biogeography of the group the composition and intergeneric relationships of the Australo-Papuan radiation remain poorly understood. Here we analysed DNA sequence data from two nuclear gene regions and the mitochondrial cytochrome b gene, for 40 species of core Corvoidea to test the systematic affinities of key Australo-Papuan lineages. The families Pachycephalidae (whistlers, shrike-thrushes and allies) and Psophodidae (whipbirds, quail-thrush and allies) were both recovered as polyphyletic assemblages. The core pachycephaline assemblage comprised Pachycephala, Colluricincla, parts of Pitohui, and Falcunculus with the remaining genera resolving as four divergent lineages with no clearly defined affinities. Ptilorrhoa and Cinclosoma (Cinclosomatidae) formed a clade separate from Psophodes (Psophodidae) but neither clade showed clear affinities to any other taxa. Novel relationships were also identified for three aberrant New Guinean genera; ditypic Machaerirhynchus and monotypic Rhagologus were both nested within an assemblage that included the Artamidae and African malaconotoids (bush-shrikes and allies) while the enigmatic Ifrita was found to be part of an assemblage that included the Monarchidae and Paradisaeidae.

Introduction

A range of molecular datasets have identified the Australo-Papuan region as the centre of diversification for the oscine passerines (e.g. Sibley and Ahlquist, 1990, Christidis and Schodde, 1991, Barker et al., 2002, Barker et al., 2004, Ericson et al., 2002a). The key assemblages within the region include the Menurae, Ptilonorhynchidae, Climacteridae, Meliphagoidea, Orthonychidae, Pomatostomidae and core Corvoidea (sensu Barker et al., 2004). The core Corvoidea is the largest and most diverse assemblage within the Australo-Papuan region and also has major radiations within Africa and Asia (Beresford et al., 2005, Jønsson and Fjeldså, 2006). The circumscription of many genera and families within the core Corvoidea, as well as their phylogenetic affinities, remain unresolved. Molecular analyses have revealed that some taxa placed within the core Corvoidea are members of other assemblages (examples in Pasquet et al., 2002, Jønsson et al., 2007, Jønsson et al., 2008a) while some genera have been shown to be polyphyletic (Jønsson et al., 2007, Jønsson et al., 2008a). Nevertheless the emerging picture is of an African-centred radiation comprising bush-shrikes, vangas and allies (malaconotoids), and an Australo-Papuan radiation comprising the monarchs, fantails and birds-of-paradise among others (Barker et al., 2004, Fuchs et al., 2004, Moyle et al., 2006).

Within the Australo-Papuan region the Pachycephalidae has not been examined in detail. This assemblage (the Pachycephalinae of Sibley and Ahlquist, 1990) has previously been considered to include sitellas (Daphoenositta), the New Zealand endemic genus Mohoua, whistlers (Pachycephala), shrike-thrushes (Colluricincla), crested bellbird (Oreoica), shrike-tit (Falcunculus), pitohuis (Pitohui) and mottled whistler (Rhagologus). Several monotypic genera – goldenface (Pachycare), olive-flanked whistler (Hylocitrea), maroon-backed whistler (Coracornis) and wattled plough-bill (Eulacestoma) – were also assigned to the Pachycephalinae (Sibley and Ahlquist, 1990) although DNA–DNA hybridization data was lacking. Preliminary molecular analyses employing multi-gene datasets have since shown that Pitohui is polyphyletic (Jønsson et al., 2008b, Dumbacher et al., 2008) and that Hylocitrea is a member of the Passerida (Jønsson et al., 2008a, Spellman et al., 2008), while Norman et al. (in press) have shown that Pachycare also lies outside the core Corvoidea and is a member of the Acanthizidae. The presumed monophyly of the remaining pachycephalines requires examination.

Another controversial assemblage within the Australo-Papuan core Corvoidea is the Psophodidae. The family currently comprises five genera restricted to Australia and New Guinea (Androphobus, Cinclosoma, Ifrita, Psophodes, Ptilorrhoa) following the demonstration that neither southeast Asian Eupetes (Jønsson et al., 2007) nor New Guinean Melampitta (Barker et al., 2004) are members of this assemblage as previously suggested (reviewed in Boles, 2007). The monophyly of the remaining members of the Psophodidae requires examination, in particular the affinities of the enigmatic New Guinean Ifrita which has proven difficult to place (see Dickinson, 2003). The relationships of the Australo-Papuan boatbills (Machaerirhynchus) also require examination. Although it is traditionally placed within the Monarchidae, microcomplement fixation data (Baverstock et al., 1992) and osteological comparisons (Schodde and Mason, 1999) indicate that this genus is a highly divergent flycatcher lineage or placed outside the Monarchidae. Irestedt et al. (2008) have recently shown that the Fijian endemic silktail Lamprolia victoriae is not a member of the Monarchidae (Olson, 1980, Sibley and Ahlquist, 1990) or Dicruridae (Sibley and Monroe, 1990, Dickinson, 2003) as traditionally accepted but is closely aligned with the Rhipiduridae.

The composition of the Artamidae (woodswallows, butcherbirds and allies) has also been revised recently. The study of Moyle et al. (2006) indicates that the Bornean bristlehead (Pityriasis) is not a member of the Artamidae as proposed by Sibley and Ahlquist (1990), but is aligned with the larger artamid–malaconotoid assemblage. The remaining artamid genera are generally regarded as comprising three lineages: (1) Cracticus, Gymnorhina, Strepera (traditionally segregated as the family Cracticidae); (2) Peltops; (3) Artamus (Schodde and Mason, 1999, Manegold, 2008) although Christidis and Boles (2008) include monotypic Gymnorhina in Cracticus. Dickinson (2003) proposed resegregating Artamus into a family on its own implying a closer affinity between Peltops and the remaining genera.

Resolution of the composition and relationships within the Australo-Papuan core Corvoidea is essential to our understanding of the biogeographical patterns across the pan-tropical region of Africa, Asia and Australasia. In order to provide better clarity on the composition and phylogenetic relationships of Australo-Papuan genera within the core Corvoidea, we analysed DNA sequence data from the nuclear recombination activating gene-1 (RAG-1), myoglobin intron II (Myo2), and the mitochondrial cytochrome b (Cyt b) gene for 61 species. The dataset included representatives of the major Australo-Papuan lineages of core Corvoidea along with several aberrant genera from this region Representatives from other Australo-Papuan centred assemblages, along with the African malaconotoids, the Vireonidae and Passerida, were included in the study to assist in better defining the phylogenetic placement of these aberrant genera and species. In particular we aimed to test (1) monophyly of the Pachycephalidae, especially the placement of Eulacestoma, Falcunculus, Mohoua and Rhagologus within this group, and the affinities of Daphoenositta (Neosittidae), (2) monophyly of the Psophodidae and placement of the enigmatic Ifrita, (3) affinities of Machaerirhynchus to the Monarchidae and (4) relationships among the three lineages of the Artamidae.

Section snippets

Taxon sampling

Our dataset comprised 61 ingroup taxa (Table 1) and included 39 species of core Corvoidea spanning the entire radiation within the Australo-Papuan region, three representatives of the African malaconotoid radiation and a member of the Vireonidae. The remaining 20 species comprised representatives from the other major lineages of Australo-Papuan oscines [Ptilonorhynchidae, Climacteridae, Meliphagoidea (Acanthizidae, Maluridae, Meliphagidae), Menuridae, Orthonychidae, Petroicidae and

Variation in the molecular dataset

The molecular dataset included 906 bp of sequence from the RAG-1 gene of which 321 sites (35%) were variable and 174 sites (19%) parsimony informative. Individual Cyt b sequences ranged from 806 to 999 bp in length. Overall, 492 sites (49%) were variable of which 444 (44%) were parsimony informative. For Myo2, we obtained 756 bp of aligned sequence (including indels) of which 435 sites (57%) were variable, and 245 sites (32%) parsimony informative. Individual Myo2 sequences varied in length from

Phylogenetic relationships among Australo-Papuan oscine passerines

The combined analysis (Fig. 4) recovered the major oscine assemblages that have been evident in previous molecular phylogenetic studies (Ericson et al., 2002a, Ericson et al., 2002b, Barker et al., 2002, Barker et al., 2004). There was strong support for the Meliphagoidea (Acanthizidae, Meliphagidae, Maluridae) and Petroicidae with the latter forming a strongly supported clade with the Passerida. The Ptilonorhynchidae, Climacteridae and Menuridae resolved as the basal lineages. In agreement

Acknowledgments

We thank V. White, M. Irestedt and D. Zuccon for laboratory assistance; W.E. Boles for editorial comments; and three anonymous reviewers for helpful comments on earlier versions of the manuscript. For the loan of tissue samples we thank the Auckland Museum (New Zealand), Australian National Wildlife Collection (Commonwealth Scientific and Industrial Research Organisation, Australia) and South Australian Museum (Australia). This research was supported by Swedish Research Council Grant No.

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