A comprehensive molecular phylogeny of the starlings (Aves: Sturnidae) and mockingbirds (Aves: Mimidae): Congruent mtDNA and nuclear trees for a cosmopolitan avian radiation

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Abstract

We generated a comprehensive phylogeny for the avian families Sturnidae (starlings, mynas, Rhabdornis, oxpeckers, and allies) and Mimidae (mockingbirds, thrashers, and allies) to explore patterns of morphological and behavioral diversification. Reconstructions were based on mitochondrial DNA sequences from five coding genes (4108 bp), and nuclear intron sequences from four loci (2974 bp), for most taxa, supplemented with NDII gene sequences (1041 bp) derived from museum skin specimens from additional taxa; together the 117 sampled taxa comprise 78% of the 151 species in these families and include representatives of all currently or recently recognized genera. Phylogenetic analyses consistently identified nine major clades. The basal lineage is comprised of the two Buphagus oxpeckers, which are presently confined to Africa where they are obligately associated with large mammals. Some species in nearly all of the other major clades also feed on or around large vertebrates, and this association may be an ancestral trait that fostered the world-wide dispersal of this group. The remaining taxa divide into sister clades representing the New-World Mimidae and Old-World Sturnidae. The Mimidae are divided into two subclades, a group of Central American and West Indian catbirds and thrashers, and a pan-American clade of mockingbirds and thrashers. The Sturnidae are subdivided into six clades. The Phillipine endemic Rhabdornis are the sister lineage to a larger and substantially more recent radiation of South Asian and Pacific island starlings and mynas. A clade of largely migratory or nomadic Eurasian starlings (within which the basal lineage is the model taxon Sturnus vulgaris) is allied to three groups of largely African species. These reconstructions confirm that Buphagus should not be included in the Sturnidae, and identify many genera that are not monophyletic. They also highlight the substantial diversity among the major Sturnidae subclades in rates of species accumulation, morphological differentiation, and behavioral variation.

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

References (71)

  • D. Amadon

    The genera of starlings and their relationships

    Am. Mus. Novitates

    (1943)
  • D. Amadon

    Remarks on the starlings, family Sturnidae

    Am. Mus. Novitates

    (1956)
  • D. Amadon

    Family Sturnidae

  • American Ornithologists’ Union, 1998. Checklist of North American Birds, seventh ed. American Ornithologists’ Union,...
  • B.S. Arbogast et al.

    The origin and diversification of Galapagos mockingbirds

    Evolution

    (2006)
  • R.C. Banks et al.

    Forty-third supplement to the American Ornithologists’ Union Checklist of North American Birds

    Auk

    (2002)
  • B.R. Barber et al.

    Systematic position of the Socorro mockingbird Mimus graysoni

    J. Avian Biol.

    (2004)
  • F.K. Barker et al.

    Phylogeny and diversification of the largest avian radiation

    Proc. Natl. Acad. Sci. USA

    (2004)
  • W.J. Beecher

    A phylogeny of the oscines

    Auk

    (1953)
  • J. Bergsten

    A review of long-branch attraction

    Cladistics

    (2005)
  • D. Brewer

    Wrens, Dippers, and Thrashers

    (2001)
  • J.K. Christians et al.

    Seasonal decline in clutch size in European starlings: a novel randomization test to distinguish between the timing and quality hypotheses

    J. Anim. Ecol.

    (2001)
  • S.M. Clegg et al.

    Genetic consequences of sequential founder events by an island-colonizing bird

    Proc. Natl. Acad. Sci. USA

    (2002)
  • M.L. Cody

    Family Mimidae (mockingbirds and thrashers)

  • P.J. Cordero et al.

    Seasonal variation in sex ratio and sexual egg dimorphism favouring daughters in first clutches of the spotless starling

    J. Evol. Biol.

    (2001)
  • A.J.F.K. Craig

    A phylogeny for the African starlings (Sturnidae)

    Ostrich

    (1997)
  • A.J.F.K. Craig

    The timing of moult, morphology, and an assessment of the races of the Redwinged Starling

    Bonn. Zool. Beitr.

    (1998)
  • A.J.F.K. Craig et al.

    The arrangement and structure of feather melanin granules as a taxonomic character in African starlings (Sturnidae)

    Auk

    (1985)
  • A.J.F.K. Craig et al.

    Biogeography and sympatry of Red-winged and Pale-winged Starlings in southern Africa

    J. Afr. Zool.

    (1992)
  • P.J. de la Cruz-Cardiel et al.

    Allozyme polymorphism and interspecific relationships in the Common starling (Sturnus vulgaris) and Spotless starling (S. unicolor) (Aves: Sturnidae)

    J. Zool. Syst. Evol. Res.

    (1997)
  • R.L. Curry et al.

    Interisland variation in blood drinking by Galápagos Mockingbirds

    Auk

    (1987)
  • J. Davis et al.

    Family Mimidae

  • K.C. Derrickson

    Variation in repertoire presentation in Northern Mockingbirds

    Condor

    (1988)
  • E.C. Dickinson

    The Howard and Moore Complete Checklist of the Birds of the World

    (2003)
  • D.L. Duffy et al.

    Song predicts immunocompetence in male European starlings (Sturnus vulgaris)

    Proc. R. Soc. Lond. B

    (2002)
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    Present address: Department of Integrative Biology and Museum of Vertebrate Zoology, University of California, Berkeley, CA 94720, USA.

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