Assessing the passerine “Tapestry”: phylogenetic relationships of the Muscicapoidea inferred from nuclear DNA sequences
Introduction
The perching birds (Order Passeriformes) represent nearly 60% of extant avian species diversity. Relationships among this vast assemblage have traditionally been uncertain as can be seen in the differences among older, widely-used classification systems (e.g., Mayr and Amadon, 1951; Mayr and Greenway, 1956; Wetmore, 1960). This situation changed dramatically with the publication of the DNA–DNA hybridization tree, the so-called “Tapestry,” of Sibley and Ahlquist (1990). Over the past decade the DNA hybridization tree has become widely used as a comparative framework to generate inferences about the evolution of ecological and behavioral traits across passerine birds, including songbirds (e.g., Owens and Bennett, 1995; Sheldon and Whittingham, 1997; Slikas, 1998).
Recently, significant advances in our understanding of passerine phylogeny have resulted from the accumulation of molecular studies employing increasingly better taxon samples (Barker et al., 2002, Barker et al., submitted; Cracraft et al., in press; Ericson et al., 2002; Irestedt et al., 2001). This work has resulted in the possibility of testing the hypotheses proposed by Sibley and Ahlquist (1990) using direct character evidence instead of phenetic distance similarity, and the aim of this paper is to re-examine the relationships within one of their primary passerine clades, the superfamily Muscicapoidea. The muscicapoids contain a large diversity of primarily Old World species within the passeridan songbirds (Barker et al., 2002; Sibley and Ahlquist, 1990); the “core muscicapoid” clade (Barker et al., 2002, Barker et al., submitted; Cracraft et al., in press) includes the waxwings, silky flycatchers, Palm Chat, dippers, starlings, mockingbirds, thrushes, chats, and Old World flycatchers. Although these birds have been generally divided into a number of families on the basis of morphological, behavioral, and ecological features, meaningful diagnostic characters are lacking. Recent molecular investigations using increased taxon samples (Barker et al., 2002, Barker et al., submitted; Cracraft et al., in press) have supported the monophyly of the “core muscicapoids.”
Several morphological studies have proposed that the waxwings, silky flycatchers, and Palm Chat (the monotypic genus Dulus) are closely related and should be included in a single family Bombycillidae (Arvey, 1951; Beecher, 1953). On the basis of egg-white proteins Sibley (1970) suggested a relationship between waxwings and silky flycatchers but not between these and the Palm Chat. Later, Sibley (1973) suggested that the silky flycatchers might be related to the turdine genus Myadestes. The results of DNA hybridization agreed with the morphological studies, and Sibley and Ahlquist (1990) divided the waxwings, silky flycatchers, and Palm Chat into three “tribes” within the Bombycillidae, and placed the family in a basal position among the Muscicapoidea (Fig. 1). The dippers (Cinclidae) comprise five species included in one genus (Cinclus); three of the species are found in the Eurasia and Africa, and two are distributed in the New World. The wrens (Troglodytidae) and thrushes (Turdidae) are usually thought to be close relatives of the dippers (Mayr and Amadon, 1951; Wetmore, 1960). Sibley (1970) suggested that egg-white protein patterns support a relationship between dippers and thrushes, but rejected a dipper–wren alliance. Using DNA hybridization Sibley and Ahlquist (1990) concluded that the cinclids are the sister-group of the muscicapid-sturnid clade and that wrens belong to another passeridan superfamily, the Sylvioidea. The starlings, mynas, and oxpeckers have usually been grouped into the Old World family Sturnidae, but there has been no consensus about their relationships to other songbirds. Earlier classifications placed them close to the Old World orioles, family Oriolidae (Amadon, 1943, Amadon, 1956; Howard and Moore, 1994) or to the weavers (Ploceidae; Berndt and Meise, 1962; Voous, 1977). Mayr and Amadon (1951) included the starlings in a group that included the Ploceidae, Oriolidae, and Dicruridae (drongos), followed by the crows and their allies (Corvidae). The mockingbirds and thrashers comprise the New World family Mimidae, and most classifications have placed them between wrens and thrushes (Mayr and Amadon, 1951; Voous, 1977; Wetmore, 1960). In contrast, some authors have argued that morphological (Beecher, 1953) and molecular data (Sibley and Ahlquist, 1984, Sibley and Ahlquist, 1990; Stallcup, 1961) support a relationship between the starlings and mockingbirds.
The thrushes, chats, and Old World flycatchers form a remarkably diverse group within the Muscicapoidea that was originally defined by the presence of spots in the juvenile plumage. For a long time these birds were grouped together in the “primitive insect eaters,” which also included a great number of Old World passerine families (Mayr and Greenway, 1956; Voous, 1977). A study of the passerine syrinx (Ames, 1975) provided an important new character for the definition of the turdine-musicapine group, namely a presumed derived pattern of the syringeal musculature (called “thumb-like”), whereas other non-muscicapid birds were found to have a generalized syrinx (Ames, 1975). Both thrushes and flycatchers are widely distributed in the Old World, but thrushes have also expanded substantially into the Americas.
This paper focuses on the large-scale phylogenetic relationships and biogeography of the Muscicapoidea superfamily, using nuclear sequences from the RAG-1 gene and an expanded taxon sample. At the same time, it provides an opportunity to assess the findings of DNA hybridization at several taxonomic scales.
Section snippets
Taxon sampling
Previous studies on passerine phylogeny included a relatively small number of muscicapoids taxa: five in Barker et al. (2002) (Cinclus, Muscicapa, Turdus, Mimus, and Sturnus), two in Ericson et al. (2002) (Mimus and Sturnus). The data set analysed here has 44 musicapoid taxa as ingroup plus six other oscine birds as outgroups.
New sequences used in this study are listed in the Appendix A and have been deposited in GenBank. Previously published sequences were also used in this study and include:
Sequence variation
Alignment of RAG-1 was straightforward, with only four indels for the total data set: one-codon deletion for the clade (Cercotrichas, Copsychus, Melaenornis, and Rhinomyias), four-codon deletion for Cinnyricinclus, one-codon deletion for Tyrannus, and a one-codon insertion for the Bombycillidae (Bombycilla and Phaenoptila). A matrix of 2875 characters was then used for all analyses (matrix submitted to EMBL database). Given this alignment, 30.8% of the sites were variable, and 16.4% were
Phylogenetics
All analyses suggest that the Muscicapoidea are composed of three main groups: the Cinclidae (dippers), the Muscicapidae sensu lato (thrushes and Old World flycatchers), and the Sturnidae sensu lato (starlings and mimids, including Buphagus and Rhabdornis). Our results agree with those of Barker et al. (2002) in finding that the Bombycillidae and allies lie outside the core Muscicapoidea and that Cinclus is the apparent sister-taxon of the thrushes and flycatchers, in contrast to the DNA
Acknowledgments
For providing tissue samples we thank Shannon Hackett and Dave Willard (Field Museum of Natural History, Chicago); Frederick Sheldon (Museum of Natural Science, Louisiana State University); Jon Fjeldså(Institute of Zoology, Copenhagen); Tim Crowe and Claire Spottiswood (Percy Fitzpatrick Institute, University of Cape Town, South Africa). A. Cibois was supported on a F.M. Chapman Postdoctoral Fellowship at the American Museum of Natural History while finishing this work. This paper is a
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