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On the Phylogenetic Position of the Scrub-Birds (Passeriformes: Menurae: Atrichornithidae) of Australia

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On the Phylogenetic Position of the Scrub-Birds (Passeriformes: Menurae: Atrichornithidae) of Australia J Ornithol (2007) 148:471^76 DOI 10.1007/S10336-007-0174-9 On the phylogenetic position of the scrub-birds (Passeriformes: Menurae: Atrichornithidae) of Australia R. Terry Chesser • José ten Have Received: 27 July 2006 / Revised: 23 October 2006 / Accepted: 2 March 2007 / Published online: 19 July 2007 © Dt. Ornithologen-Gesellschaft e.V. 2007 Abstract Evolutionary relationships of the scrub-birds Introduction Atrichornis were investigated using complete sequences of the recombination-activating gene RAG-1 and the proto- The Australian endemic family Atrichornithidae consists of oncogene c-mos for two individuals of the noisy scrub-bird two species of small passerine bird: the noisy scrub-bird Atrichornis clamosus. Phylogenetic analysis revealed that Atrichornis clamosus (Gould 1844), an inhabitant of scrub Atrichornis was sister to the genus Menura (the lyrebirds) and dry forest in southwestern Australia, and the rufous and that these two genera (the Menurae) were sister to the scrub-bird A. rufescens (Ramsay 1866), found in subtrop- rest of the oscine passerines. A sister relationship between ical rainforests of eastern Australia. Both are ground- Atrichornis and Menura supports the traditional view, dwelling species of limited distribution, highly secretive based on morphology and DNA hybridization, that these and uncommon within their respective ranges; indeed, taxa are closely related. Similarly, a sister relationship with A. clamosus was considered extinct for many decades prior the remaining oscine passerines agrees with the morpho- to its rediscovery in 1961 (Webster 1962a, b). logical distinctiveness oí Atrichornis and Menura, although John Gilbert, collector of the first specimens of A. this result contradicts conclusions based on DNA hybrid- clamosus, considered the scrub-birds to be similar to the ization studies. Although Atrichornis is very well known bristlebirds (genus Dasyornis), with whom they share morphologically, previous conclusions regarding its rela- ecological, behavioural and vocal features, and this was tionships were hampered by a lack of comparative their original taxonomic placement (Gould 1865). They knowledge of other passerines, making concurrence of the have also been considered to be closely related to other sequence data of particular significance. Australian ground-dwelling taxa, including the whipbirds (genus Psophodes; Chisholm 1951). For the past century, Keywords Atrichornis • Menurae • Passeriformes • however, most systematists have considered scrub-birds to Phylogenetics • Scrub-birds be the sister group to the lyrebirds (genus Menura, family Menuridae), a relationship first promulgated by Garrod (1876). Communicated by M. Wink. The broader relationships of Atrichornis have also re- ceived considerable attention. Garrod (1876) proposed a R. T. Chesser • J. ten Have separate grouping within the oscines, the Acromyodi Ab- Australian National Wildlife Collection, normalis, for Atrichornis and Menura, with the remainder CSIRO Sustainable Ecosystems, of the songbirds forming the Acromyodi Normalis. Sclater GPO Box 284, Canberra, ACT 2601, Australia (1880) went further, characterizing Atrichornis and Men- Present Address: ura as "the most anomalous forms of Passerine birds yet R. T. Chesser (El) known" and considering them to constitute a suborder of USGS Patuxent Wildlife Research Center, Passeriformes removed from the oscines. This arrangement National Museum of Natural History, PO Box 37012, Washington D.C. 20013, USA was followed by most ornithologists over the next e-mail: [email protected] 100 years (e.g., Mayr and Amadou 1951; Wetmore 1960), •Ö Springer 472 J Ornithol (2007) 148:471^76 although many morphologists (see Bock and Clench 1985) at 13,000 rpm for 10 min. The pellet was washed with 70% considered Atrichornis and Menura to be oscine. ethanol and air-dried before resuspending in 50-100 \ú Sibley's (1970, 1974) studies of egg-white proteins did O.lx TE/10 (ig/ml RNaseA. not include Atrichornis, but indicated that the lyrebirds Following Barker et al. (2002), we sequenced two nu- were oscines closely related to the bowerbirds clear exons - the recombination-activating gene RAG-1 (Ptilonorhynchidae) and birds of paradise (Paradisaeidae), (Schatz et al. 1989; Carlson et al. 1991) and the proto- and he suggested that the suborder Menurae (consisting of oncogene c-mos (Schmidt et al. 1988; Saint et al. 1998) - Menura and Atrichornis) be merged into the oscines. Re- for two individuals of A. clamosus. The primers used for sults of his subsequent DNA hybridization studies (Sibley amplification and sequencing have been published previ- and Ahlquist 1985, 1990) indicated that Atrichornis and ously (Groth and Barrowclough 1999, Barker et al. 2002), Menura were oscine birds embedded within the parvorder except for 13C (5'-TCTGAATGGAAATTCAAGCTCTT- Córvida and that their nearest relatives were the bowerbirds 3') and R659L (5'-GTCAAGAGAAAAAGCCAGCCC-3'), (which the hybridization evidence indicated were not clo- developed by J.G. Groth. Primer pairs used to amplify sely related to the birds of paradise). RAG-1 (13C/18, 17/22 and 21/21) were chosen to generate Recent studies of passerines based on DNA sequence three overlapping fragments. All amplifications were per- data (Barker et al. 2002, 2004; Ericson et al. 2002a, b) have formed on an Eppendorf Mastercycler (gradient) in 200-(il found important differences compared to the DNA hybrid- striptubes, using a 50-|j,l reaction volume containing ization results (Sibley and Ahlquist 1985, 1990), especially 200 iiM dNTPs, 1.5 mM MgClj, 50 pmol of each of the in terms of the early radiations of Australasian songbirds. primers, Ix PCR buffer and 0.5 U Taq DNA polymerase The results of these studies, for example, showed the (Gibco-BRL, Gaitersburg, Md.). RAG-1 ampUfications Córvida (Sibley and Ahlquist 1985, 1990) to be a were conducted using a step-down PCR protocol: five cy- paraphyletic grade basal to other oscines, the most basal cles of denaturing at 96°C for 20 s (4 min in cycle 1), branches of which consisted exclusively or largely of annealing at 58°C for 15 s and extension at 72°C for 1 min; Australasian taxa. Within this context, Menura was found to five cycles with annealing at 56°C; five cycles with be sister to all other oscines. However, these studies were annealing at 54°C; 25 cycles with annealing at 52°C, fol- unable to incorporate sequence data from the genus Atri- lowed by a final extension of 5 min. C-mos was amplified chornis. In this paper, we use DNA sequence data from the using primers CM5 and CM6 under the following condi- noisy scrub-bird, A. clamosus, to address the relationships of tions: five cycles of denaturing at 96°C for 20 s (4 min in the scrub-birds both to Menura and, more generally, within cycle 1), annealing at 65°C for 30 s, extension at 72°C for the Passeriformes and to compare these results to those of 1 min; 30 cycles with annealing at 60°C, followed by a studies based on morphology and DNA hybridization. final extension of 5 min. The PCR products were visual- ized on an agarose gel and purified using the Qiagen gel extraction kit (Valencia, Calif.). The L-strand and H-strand Methods were sequenced for both genes. RAG-1 primers 13C, 15, 23, 17, 19, R659L and 21 were used to sequence the L- Blood samples from individuals of A. clamosus, captured strand, and RAG-1 primers 16, 18, 21, 20, 22, and 24 to for translocation by the Western Australian Department of sequence the H-strand. C-mos sequencing was performed Conservation and Land Management (CALM), were do- using the amplification primers CM5 and CM6. Sequenc- nated to the Australian National Wildlife Collection ing was conducted using dye-terminator chemistry on an (ANWC). DNA was extracted from two samples (01 MOI ABI 377 automated sequencer (Applied Biotechnologies, and 01M04; ANWC 10646 and 10649, respectively) using Foster City, Calif.). All sequences obtained for A. clamosus the CTAB DNA extraction method (Doyle and Doyle have been deposited in GenBank (accession numbers 1987), with modifications as described below. A small EF463007-EF463010). amount of blood, previously preserved in EtOH, was Sequences were aligned and edited in SEQUENCHER ver. placed in a 1.5-ml tube with 300 \ú of 2x CTAB buffer in 4.1 (GeneCodes 2000) and combined with the data set of the presence of Proteinase K (20 mg/ml) at 20 |j,l/500 (il Barker et al. (2002). Phylogenetic analyses of the resulting CTAB and /?-mercapto-ethanol (0.6 p,l/300 |j,l). This was 73-taxon data set were conducted using PAUP* ver. 4.0b 10 incubated at 60°C overnight. The mixture was then ex- (Swofford 2002) on the combined and individual genes. The tracted twice with equal volumes of CHCL3:IAC (96:4) 36-base ambiguous region of c-mos (Barker et al. 2002) was and centrifuged for 5-10 min at 13,000 rpm. The DNA excluded from the analyses. Tree searches were performed was precipitated through the addition of 0.1 vol. 3 M using maximum parsimony and maximum likelihood (ML) NaOAc and 2.5 vol. EtOH (RT), mixed by inversion, methods, with Callus designated the outgroup in all anal- incubated at RT for approximately 2 min and centrifuged yses. Parsimony searches were conducted using 500 random ö Springer J Ornithol (2007) 148:471^76 473 addition replicates. Character support for parsimony-based Acanthisitta chloris phylogenies was assessed via bootstrapping (Felsenstein other oscines 1985), using 100 heuristic searches with ten random addi- 99 Malurus melanocephalus tion replicates each, and branch support (Bremer 1988, 10 76 97 1994), which was computed using the computer programme Mellphaga análoga 99 2 11 TREEROT ver. 2 (Sorenson 1999). Likelihood analyses were 13 Pardalotus striatus conducted on the combined data using the parameters ob- 100 97 Climacteris picumnus tained from the computer programme MODELTEST (Posada 31 7 Ptilonorhynchus violáceas and Crandall 1998).
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