Nuclear and mitochondrial sequence data reveal the major lineages of starlings, mynas and related taxa

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Abstract

We investigated the phylogenetic relationships among the major lineages of the avian family Sturnidae and their placement within the Muscicapoidea clade using two nuclear (RAG-1 and myoglobin) and one mitochondrial gene (ND2). Among Muscicapoidea, we recovered three clades corresponding to the families Cinclidae, Muscicapidae and Sturnidae (sensu [Sibley, C.G., Monroe Jr., B.L., 1990. Distribution and Taxonomy of Birds of the World. Yale University Press, New Haven, CT]). Within the sturnoid lineage Mimini and Sturnini are sister groups, with Buphagus basal to them. We identified three major lineages of starlings: the Philippine endemic genus Rhabdornis, an Oriental-Australasian clade (genera Scissirostrum, Gracula, Mino, Ampeliceps, Sarcops, Aplonis), and an Afrotropical-Palaearctic clade (all African taxa, Sturnus and Acridotheres). We discuss the biogeographic implications of our findings and suggest an Asiatic origin for this family. The congruence between the age of major clades, estimated by NPRS, and palaeoclimatic data present evidence for the role of climatic changes in shaping present day distribution of the group.

Introduction

Most recent studies of passerine relationships suggest that this group began to diversify already during the Cretaceous (Barker et al., 2002, Barker et al., 2004, Ericson et al., 2002). Despite this long time for diversification the passerines show a remarkable anatomical uniformity, except for structures adapted for feeding and locomotion (e.g. Irestedt et al., 2004). Similar morphologies resulting from the occupation of the same ecological niches by representatives of different phylogenetic lineages of passerines have been notoriously difficult to separate from similarities due to a recent common ancestry. This has led avian taxonomists to group many taxa that are now known to be unrelated (cf. Sibley and Ahlquist, 1990).

The starlings (Sturnini sensu [Sibley and Monroe, 1990]) constitute one example of a group in which the internal affinities are misunderstood due to several cases of morphological convergence. The starlings are distributed in the Old World (one species has been introduced in the New World). They are small to medium-sized birds, robustly built, with quite long wings, strong legs and feet and usually a short tail. The sexes are alike and the young are usually rather different from the adults (Feare and Craig, 1998, Fry and Keith, 2000). It has been a long practice to associate starlings with crows and allies (Corvidae), icterids (Icteridae), or weaverbirds (Ploceidae), because of their bulky body shape, strong bill and often dark/black glossy plumage (Gray, 1840, Gray, 1870; Bonaparte, 1850–1857; Sharpe, 1890, Sharpe, 1891, Sharpe, 1909, Wetmore, 1930, Mayr and Greenway, 1956, Voous, 1977). A relationship with corvids was dismissed by Bock (1962) since starlings like other non-corvidian passerines have two fossae in the proximal end of the humerus, not a single fossa as in corvids.

Based on analyses of DNA–DNA hybridization data, Sibley and Ahlquist (1990) recognised three major lineages among oscine passerines. One of them, the superfamily Muscicapoidea, comprises four families; Bombycillidae (waxwings, silky flycatchers, palm chat), Cinclidae (dippers), Muscicapidae (thrushes in subfamily Turdinae, Old World flycatchers and chats in subfamily Muscicapinae), and Sturnidae. Sturnidae was further divided into the tribes Sturnini (starlings) and Mimini (mockingbirds). The latter result was especially surprising, although a starling–mockingbird relationship had been proposed earlier based on morphology (Beecher, 1953), serological complement fixation (Stallcup, 1961) and egg-white protein similarities (Sibley, 1970). Although all higher-level relationships of passerines suggested by Sibley and Ahlquist (1990) have not been supported by subsequent studies (Harshman, 1994, Sheldon and Gill, 1996, Ericson and Johansson, 2003, Barker et al., 2004), the monophyly of a “core Muscicapoidea” (i.e. Sibley’s group waxwings and allies excepted) is now generally accepted.

However, many internal relationships in Muscicapoidea are less clear and phylogenetic hypotheses differ depending on which dataset is analysed. It has proven especially difficult to determine the sister group of Sturnidae and the position of Cinclidae. Nuclear datasets (Cibois and Cracraft, 2004, Barker et al., 2004, Beresford et al., 2005) agree with the results based on DNA–DNA hybridization data in placing Sturnidae as sister to a Cinclidae–Muscicapidae clade but the position of Bombycillidae, basal to all other Muscicapoidea, is supported only in a few analyses in Barker et al. (2004). Analysis of a combination of mitochondrial and nuclear data instead suggests that Cinclidae and Sturnidae are sisters and that they are most closely related to Turdinae (Voelker and Spellman, 2004). According to this dataset Muscicapinae belong to a separate clade, whereas the Bombycillidae are not part of Muscicapoidea at all (Voelker and Spellman, 2004).

The tribe Sturnini is a rather well-defined taxon, including 114 extant and 5 extinct species in 29 genera (Sibley and Monroe, 1990). Starlings occur in Africa, Eurasia, across the Wallacea to New Guinea and in most Pacific islands, but only marginally in Australia. There are two main biodiversity centers in Sturnini: in the sub-saharan Africa and in the Oriental-Australasian regions (Feare and Craig, 1998). Most recent studies used an insufficient taxon sampling to properly address intergeneric relationships and the starling diversification is poorly understood. Conflicting hypotheses in the literature concern for example the postulated relationship between Scissirostrum and Buphagus (Beecher, 1978), whether SturnusAcridotheres are the sister group of LamprotornisCinnyricinclus or actually nested within it (Sibley and Ahlquist, 1990, Cibois and Cracraft, 2004), and the proposed monophyly of the Afrotropical taxa (Craig, 1997).

Several enigmatic taxa have been allied with the starlings in the past, like the bush-crow Zavattariornis stresemanni and the huia Heterolocha acutirostris. Both these have been shown to belong to the corvid assemblage (Barker et al., 2004, Ericson et al., 2005). Recently the Philippine genus Rhabdornis, a taxon never thought to be close to starlings, was identified as the sister group of Sturnidae (Barker et al., 2004, Cibois and Cracraft, 2004). These poorly known, small arboreal birds are found only in the Philippines where they are rather common in lowland and montane forests. Rhabdornis has a vague resemblance to Certhia creepers and has accordingly often been placed in Certhiidae (e.g. Sharpe, 1903).

In the present paper we use a combination of nuclear and mitochondrial genes to investigate the evolutionary and biogeographic history of the starlings. We also aim at determine which taxa should be included in the family and to calculate the age of the diversification of the major lineages in Sturnidae. The role of climate changes in driving the diversification of the family will also be explored.

Section snippets

Taxon sampling strategy

Taxon sampling in this study was designed in order to: (1) test the monophyly of the starlings (Sturnidae sensu [Sibley and Monroe, 1990]) and the general placement of this group within the Muscicapoidea clade, and (2) identify the major lineages within the starling clade. The dataset consists of 49 taxa (Table 1). The ingroup comprises 29 starling species, representing all major morphological and ecological types. Two species of Rhabdornis have been included, following the findings of Cibois

Gene properties

The final alignment of the three concatenated genes is 4670 bp long. A summary of molecular properties of each gene is shown in Table 2. The proportions of potentially informative characters are 13%, 19% and 53% in RAG-1, myoglobin, and ND2, respectively, but they decrease to 10%, 14% and 50% when only ingroup taxa are considered. Base compositions are more A and C skewed in the mitochondrial ND2 gene than in the nuclear genes. A χ2 analysis of base frequencies across taxa could not reject a

Phylogenetics

This study confirms previous studies that starlings are part of the monophyletic clade Muscicapoidea, together with mockingbirds, thrushes, chats, and flycatchers (Sibley and Ahlquist, 1990, Ericson and Johansson, 2003, Voelker and Spellman, 2004, Cibois and Cracraft, 2004, Barker et al., 2004). Waxwings and goldcrests (families Bombycillidae and Regulidae) are recovered with high support as sister branch to the “core Muscicapoidea”, an arrangement that has never been identified before. Regulus

Acknowledgments

We are grateful to the institutions and curators that provided some of the samples used in this study: Joel Cracraft and Paul Sweet (American Museum of Natural History, New York), Jon Fjeldså and Jan Bolding Kristensen (Zoological Museum, University of Copenhagen), Scott Edwards and Sharon Birks (Burke Museum, University of Seattle), David Willards (Field Museum of Natural History, Chicago), Janet Hinshaw (University of Michigan, Museum of Zoology), and Andreas Helbig (Vogelwarte Hiddensee,

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