A comprehensive molecular phylogeny of the starlings (Aves: Sturnidae) and mockingbirds (Aves: Mimidae): Congruent mtDNA and nuclear trees for a cosmopolitan avian radiation
Introduction
The Mimidae and Sturnidae are avian sister radiations that show striking parallels in a number of ecological and behavioral traits. The Sturnidae (Starlings and Mynas) are restricted to the Old World (except for human-mediated introductions elsewhere), with centers of diversity in Southeast Asia and Africa. The Mimidae have diversified in southwestern North America, the West Indies, and Central/South America and its satellite islands. Although taxa in both groups continue to serve as models in studies of behavioral (e.g., Derrickson, 1988, Kroodsma and Byers, 1991, Pinxten et al., 2002, Duffy and Ball, 2002, Gentner and Margoliash, 2003, Polo et al., 2004, Rubenstein, 2007a) and life history trait evolution (e.g., Ricklefs and Williams, 1984, Cordero et al., 2001, Christians et al., 2001, Komdeur et al., 2002, Rubenstein, 2007b), neither group has previously been the subject of phylogenetic analysis with robust taxonomic sampling. Here, we use a combination of mtDNA and nuclear DNA sequences to explore the phylogenetic relationships of all genera and most species within this cosmopolitan avian radiation.
Despite earlier evidence from studies of jaw musculature and cranial osteology (Beecher, 1953), and seriology (Stallcup, 1961), the sister relationship of the Sturnidae and Mimidae was not broadly recognized until it was featured in the DNA–DNA hybridization studies of Sibley and Ahlquist, 1980, Sibley and Ahlquist, 1990. Although this finding initially met with controversy, subsequent phylogenetic studies based on DNA–DNA hybridization (Sheldon and Gill, 1996), physiological traits (Malcarney et al., 1994), and various mitochondrial and nuclear DNA sequence loci (Voelker and Spellman, 2004, Ericson and Johansson, 2003, Cibois and Cracraft, 2004, Barker et al., 2004, Zuccon et al., 2006) have been completely concordant in grouping the Mimidae and Sturnidae as sister clades, usually with very strong topological support.
The reliable characterization of the full set of taxa that fall within a monophyletic Sturnidae/Mimidae group has been strengthened by recent phylogenetic surveys of related passerine songbird groups, particularly an intensively sampled study (Cibois and Cracraft, 2004) of the deeper Muscicapoidea radiation within which the Sturnidae and Mimidae are nested. Cibois and Cracraft (2004) included many taxa that had not been sampled previously in any molecular phylogenetic analysis, and thereby helped confirm that all major lineages within the Sturnidae/Mimidae clade have been assigned correctly to this group. Their most surprising finding involving the Sturnidae/Mimidae was the recognition that Rhabdornis, a genus endemic to the Phillipines with previously uncertain family-level affinities, is a morphologically aberrant member of the Sturnidae. A phylogenetic enigma involving a second morphologically unusual genus, the Buphagus oxpeckers of Africa, remains somewhat less well resolved. Buphagus has been variously treated as its own family (Buphagidae), or more commonly included within the family Sturnidae. All molecular phylogenies that have included the Buphagus lineage have placed it as a long branch at the base of the Sturnidae/Mimidae clade (e.g., Cibois and Cracraft, 2004, Zuccon et al., 2006), but with low support for distinguishing whether it is the basal lineage in this entire group, or alternatively the sister lineage to either the Sturnidae or Mimidae.
Less is known about relationships within and among the major subclades of the Sturnidae/Mimidae radiation. Although most of the species, as well as all of the genera, of Mimidae have been included in previous DNA-based phylogeographic or phylogenetic studies (Sibley and Ahlquist, 1990, Zink et al., 1997, Zink et al., 1999, Zink et al., 2001; Zink and Blackwell-Rago, 2000, Hunt et al., 2001, Sgariglia and Burns, 2003, Barber et al., 2004, Cibois and Cracraft, 2004, Arbogast et al., 2006), these previous reconstructions have each primarily addressed relationships among sets of closely allied species and no single reconstruction has included a complete sample of Mimidae genera. The few previous DNA-based studies of relationships within the Sturnidae have similarly been taxonomically circumscribed. For example, the most inclusive survey of Sturnidae (Zuccon et al., 2006) sampled only 30 (of 117) Sturnidae species along with 6 (of 34) Mimidae species, and did not include many genus-level lineages with long-debated affinities.
Here, we use a combination of mitochondrial (mtDNA) and nuclear DNA sequences to reconstruct the phylogenetic relationships of all well-differentiated lineages within the Sturnidae/Mimidae. By using both modern, high-quality blood and tissue samples and skin-snips taken from dried museum specimens, we included 117 of 151 (78%) taxa representing all extant genera recognized by any recent taxonomic revision, and multiple species from most polytypic genera. From the high-quality samples, we obtained substantial mitochondrial DNA (4108 bp of protein-coding gene sequence) and nuclear intron (4 loci, 2974 aligned bp) sequences, to which we added shorter (NDII only, 1041 bp) sequences from samples derived from museum skin source materials. The majority of nodes in the resulting phylogenetic reconstructions have high topological support and provide strong evidence for the historical pattern of diversification in this world-wide avian radiation.
Section snippets
Taxon sampling
We designed our taxonomic sampling strategy to include at least one representative of all morphologically or biogeographically distinctive lineages in the Sturnidae and Mimidae, including representatives of all genera recognized by any of the five most influential taxonomic treatments of the Sturnidae of the past half-century (Table 1). Here we employ the nomenclature of the most recent “Howard and Moore” checklist (Dickinson, 2003), which recognizes 26 genera and 114 extant species of
Sequence characteristics
Sequence alignments were straightforward except for one 6–12 bp region in each of the Fib-5, Fib-7, and Rho-1 intron comparisons, each of which involved single-nucleotide repeats of variable length that had unusually high insertion/deletion mutation rates leading to substantial homoplasy. Excluding these short regions of questionable alignment, we found a total of 66 indels among the ingroup taxa, of which 43 were present in more than one taxon and therefore represent potential synapomorphies.
Major clades
All reconstructions were consistent in defining three major clades within the combined Sturnidae/Mimidae radiation (summarized in Fig. 5). These three clades correspond taxonomically to the families Buphagidae, Mimidae, and Sturnidae. They can be further subdivided into two major subclades within the Mimidae and six within the Sturnidae.
Acknowledgments
Genetic samples were kindly provided by: Alain Hennache (Muséum National Histoire Naturelle, Parc de Clères); Brian Arbogast (Humboldt State University); Charles Foley (Tarangire Elephant Project); Chris Iles (Birdtrek); David Rimlinger (San Diego Zoo); David Willard and John Bates (Field Museum of Natural History); Denis O’Meally (The Australian Museum); Donna Dittmann, Van Remsen, and Frederick Sheldon (Museum of Natural Science, Louisiana State University); Eldredge Bermingham (Smithsonian
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Present address: Department of Integrative Biology and Museum of Vertebrate Zoology, University of California, Berkeley, CA 94720, USA.