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Voelker and Spellman.Pdf MOLECULAR PHYLOGENETICS AND EVOLUTION Molecular Phylogenetics and Evolution 30 (2004) 386–394 www.elsevier.com/locate/ympev Nuclear and mitochondrial DNA evidence of polyphyly in the avian superfamily Muscicapoidea Gary Voelker* and Garth M. Spellman Barrick Museum of Natural History, Box 454012, University of Nevada Las Vegas, 4505 Maryland Parkway, Las Vegas, NV 89154, USA Received 26 November 2002; revised 7 May 2003 Abstract Nucleotide sequences of the nuclear c-mos gene and the mitochondrial cytochrome b and ND2 genes were used to assess the monophyly of Sibley and MonroeÕs [Distribution and Taxonomy of Birds of the World, Yale University Press, New Haven, 1990] Muscicapoidea superfamily. The relationships and monophyly of major lineages within the superfamily, as well as genera mem- bership in major lineages was also assessed. Analyses suggest that Bombycillidae is not a part of Muscicapoidea, and there is strongly supported evidence to suggest that Turdinae is not part of the Muscicapidae, but is instead sister to a Sturnidae + Cinclidae clade. This clade is in turn sister to Muscicapidae (Muscicapini + Saxicolini). Of the 49 Turdinae and Muscicapidae genera that we included in our analyses, 10 (20%) are shown to be misclassified to subfamily or tribe. Our results place one current Saxicolini genus in Turdinae, two Saxicolini genera in Muscicapini, and five Turdinae and two Muscicapini genera in Saxicolini; these relationships are supported with 100% Bayesian support. Our analyses suggest that c-mos was only marginally useful in resolving these ‘‘deep’’ phylogenetic relationships. Ó 2003 Published by Elsevier Science (USA). Keywords: Bombycillidae; Cinclidae; Molecular systematics; Muscicapidae; Muscicapoidea; Sibley and Ahlquist; Sturnidae 1. Introduction been elevated to family status, leaving only the Old World groups Saxicolini and Muscicapini as elements of The avian family Muscicapidae has had a long hi- the Muscicapidae. story of revision. One generally consistent treatment Many of the proposed placements of groups in and throughout these revisions has been the identification of around the Muscicapidae relied on evidence of shared a core group, consisting of the Turdinae (thrushes), features such as jaw musculature, juvenal plumages, Muscicapinae (chats (Saxicolini) and muscicapine fly- tarsal scutellation, and the presence or absence of rictal catchers (Muscicapini)) and sylviine warblers (e.g., bristles (summarized in Sibley and Ahlquist, 1990). AOU, 1983; Hartert, 1910; Mayr and Amadon, 1951; However, the validity of using some of these features as Ripley, 1952). However, Muscicapidae has at various taxonomic characters has been questioned (e.g., Sibley times included, among others, such morphologically and Ahlquist, 1990) due, for example, to convergence on diverse groups as the Timaliinae (babblers), Polioptili- ecotypes or to characters being tied to foraging habits. nae (gnatcatchers), Malurinae (fairy wrens), Sylviinae Further, a number of these characters have a chaotic (Old World flycatchers), and Cinclidae (dippers) (e.g., distribution across taxa such that features attributed to Hartert, 1910; Mayr and Amadon, 1951; Storer, 1971). families generally offer no clear guide to relationships At the other extreme, under the current treatment by the (Sibley and Ahlquist, 1990). Either the characters are not American OrnithologistsÕ Union (1998), Turdinae has found in all members of a family, or the characters are not unique to single families (Sibley and Ahlquist, 1990). It was not until the DNA–DNA hybridization work * Corresponding author. Present address: Department of Biology, University of Memphis, 3700 Walker Avenue, Memphis, TN 38152, of Sibley and Ahlquist (1990), that a sweeping study USA. of passerine family relationships was conducted, E-mail address: [email protected] (G. Voelker). and an expansive phylogenetic hypothesis of ‘‘true’’ 1055-7903/$ - see front matter Ó 2003 Published by Elsevier Science (USA). doi:10.1016/S1055-7903(03)00191-X G. Voelker, G.M. Spellman / Molecular Phylogenetics and Evolution 30 (2004) 386–394 387 membership in Muscicapidae existed. The result of this subunit 2 (ND2) and 998 bp of cytochrome b (2643 bp work was the formation of a Muscicapoidea superfam- total) from 23 taxa representing all Muscicapoidea ily. Included in this superfamily were Muscicapidae families, as well as from 7 Sylvioidea taxa and 7 Passe- (Turdinae + Muscicapinae), Bombycillidae (waxwings roidea taxa (see Appendix A). We also included for and allies), Cinclidae (dippers), and Sturnidae (starlings these taxa a 604 bp segment of the nuclear c-mos gene, to (Sturnini) and thrashers (Mimini)). The explicit set of add an independent (from the single linkage unit relationships within Muscicapoidea proposed by Sibley mtDNA genes) data partition. These data have been and Ahlquist (1990) suggests a sister relationship be- submitted to GenBank under the following accessions: tween Turdinae and Muscicapinae (Saxicolini + Musci- submission in progress. capini), with Sturnidae, Cinclidae, and Bombycillidae To further assess the monophyly of Muscicapidae being progressively more distant. and to assess the monophyly of the major subclades Of the families included in Muscicapoidea by Sibley Turdinae, Muscicapini, and Saxicolini we increased our and Ahlquist (1990), only the Bombycillidae had never, sampling to include 49 genera from those groups (see to our knowledge, previously been considered part of Appendix A). This sampling included 21 of 24 pur- ‘‘Muscicapidae’’ in taxonomic treatments. And in fact, ported Turdinae genera, 9 of 17 presumed Muscicapini due to conflicting evidence in their results Sibley and genera, and 19 of 31 genera currently assigned to Sax- Ahlquist were ultimately unconvinced of their decision icolini (see Appendix A). We also included as outgroups to place Bombycillidae in Muscicapoidea, rather than in the seven Sylvioidea and seven Passeroidea taxa dis- either Sylvioidea or Passeroidea (1990; p. 630). Recent cussed above. We analyzed sequence data from the ND2 evidence from nuclear genes suggests that Bombycillidae (1041 bp) and cytochrome b (1000 bp) genes for this set is not in fact part of Muscicapoidea (Barker et al., 2001). of taxa. These additional muscicapid data are part of Confusion over relationships in Muscicapoidea is not on-going studies of inter- and intra-generic studies of limited to these higher taxonomic categories. There has Muscicapoidea relationships, and will be submitted to been a long history of revisions dealing with the true GenBank at the conclusion of those studies. Requests membership of genera in either the Turdinae, Saxicolini, for these data should be addressed to the senior author. or Muscicapini, validity of genera within those groups, as well as revisions dealing with species membership in 2.2. Sequence data given genera (e.g., Dowsett and Dowsett-Lemaire, 1993; Orenstein, 1979; Ripley, 1952, 1962; Vaurie, 1953, We extracted total genomic DNA from all tissue and 1955a,b). For example, Monticola is usually placed near blood samples using a Qiaquick tissue extraction kit Turdus in the true thrushes (Turdinae), but some au- (Qiagen; see Appendix A for sample types). The cyto- thors place Monticola in Saxicolini due to the chat-like chrome b gene was amplified using the primers L14841 behavior of several species (Vaurie, 1955a). (Kocher et al., 1989) and H4A (Harshman, 1996) and In this paper, we use a combination of nuclear and sequenced using the primers L14841 and H15299 (Ko- mitochondrial genes to explore several issues relating to cher et al., 1989); B3, B4, and B5 (Lanyon, 1994); the superfamily Muscicapoidea. First, we seek to test the L15114, L15609, and H15547 (Edwards et al., 1991); monophyly of Muscicapoidea. Second, we seek to test and H4A. We amplified the ND2 gene using the primers the family relationships proposed by Sibley and Ahl- L5215 (Hackett, 1996) and H6313 (Johnson and quist (1990), with a main interest in determining whether Sorenson, 1998) and sequenced using L5215, L5758, Muscicapidae (Turdinae, Saxicolini, and Muscicapini) is H5776, and H5578 (Hackett, 1996; Johnson and monophyletic. Finally, we seek to determine whether Sorenson, 1998); L5758.2 (Voelker, 2002); and H6313. each subgrouping within Muscicapidae is monophyletic The nuclear c-mos gene was amplified and sequenced with respect to the taxonomy proposed by Sibley and using primers 944 and 1550 (Lovette and Birmingham, Monroe (1990). 2000). All fragments were amplified in 50 ll reactions under the following conditions: denaturation at 94 °C, followed by 40 cycles of 94 °C for 30 s, 54 °C for 45 s, 2. Materials and methods and 72 °C for 2 min. This was followed by a 10 min extension at 72 and 4 °C soak. Products were purified 2.1. Specimens using a Qiagen PCR Purification Kit following manu- facturerÕs protocols. We performed 20 ll BigDye (ABI) Our sampling schemes were generally based on results sequencing reactions using 20–40 ng of purified and from the DNA–DNA hybridization studies of Sibley concentrated PCR product and following standard ABI and Ahlquist (1990) and the taxonomy of Sibley and protocols. Sequencing reactions were purified using Monroe (1990). To assess the monophyly of, and family Centrisep columns following manufacturerÕs protocols, and subfamily relationships within, Muscicapoidea, we dried in a centrivap concentrator, and run out on a used 1041 base pairs (bp) of NADH dehydrogenase Long Ranger (BMA) acrylamide gel with an ABI 377 388 G. Voelker, G.M.
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