Origin and diversification of Philippine bulbuls
Introduction
Oceanic island archipelagos provide a unique microcosm for studies of diversification. The stark geographic boundaries and comparatively simple floras and faunas remove many confounding factors present in continental regions. The Philippine archipelago, comprising over 7000 islands, is one of the largest on Earth, yet relatively little is known about the origins and diversification history of most of its endemic flora and fauna. A basic question of all archipelagoes, and the Philippines in particular, is the relative importance of colonization and in situ diversification in forming insular biotas. Among Philippine vertebrates, reptiles, amphibians, and mammals show high levels of endemism, suggesting a substantial role for diversification within the archipelago (Kennedy et al., 2000, Ong et al., 2002). This is supported by phylogenetic studies of select clades within these groups (e.g., Evans et al., 2003, Jansa et al., 2006, McGuire and Kiew, 2001). In contrast, birds show relatively low levels of endemism and suggest, in keeping with their volant nature, that colonization may be a more important driver of species diversity. That is, origins of the Philippine bird fauna involved more assembly whereas other vertebrate faunas involved greater diversification.
The Philippine archipelago has had a complex geological history but the major stages are now fairly well understood as summarized in Hall (2002) and Yumul et al. (2008). The western islands of Palawan and Mindoro are composed of continental crust that rifted from the margins of southern China and rafted to their current position. Most or all of this land was probably submerged at some point during the transit across the South China Sea. Parts of Mindanao—the Zamboanga Peninsula and the Daguma Range in the southwest—also have continental origins. These fragments were in isolation for a long period of time but they have been in contact with central Mindanao since the middle Miocene. The rest of the archipelago is oceanic, arising de novo since the late Cretaceous and throughout the Cenozoic from a complex system of island arcs between the Eurasian and the Philippine Sea plates. Individual fragments have moved in a dynamic fashion, changing direction and pace, but this belt of oceanic islands has been moving in a general northwesterly direction since the early Cenozoic. During the last glacial maximum in the Pleistocene, sea levels are estimated to have been 120 m below current levels exposing land connections between some Philippine islands (Heaney, 1986, Voris, 2000; Fig. 1).
Early workers traced the origins of Philippine bird fauna to the Sunda, Palearctic and Australasian regions (e.g., Dickerson, 1928). The Sunda region is considered the chief colonization source (Dickinson et al., 1991) and the Palawan group of islands and the Sulu archipelago are seen as important invasion routes to the Philippines (Diamond and Gilpin, 1983). The dominant framework in the study of diversification of Philippine fauna in the last two decades has been that Pleistocene islands during the last glacial maximum define the limits of homogenous populations, each of which is a center of endemism (Heaney, 1986). These patterns of colonization and diversification have been studied in a phylogeographic context in birds for a few species (Jones and Kennedy, 2008a, Jones and Kennedy, 2008b) but no thorough investigations have been carried out at higher taxonomic levels.
Bulbuls (Pycnonotidae) are ubiquitous residents of the tropical and semi-temperate Old World and are ideal subjects to study colonization and diversification patterns in the Philippines. Bulbuls are found throughout Southeast Asia, with high species richness in the Sunda region (e.g., 22 species on Borneo). They include some of the commonest species in SE Asian forests, and comprise a sizable proportion of the species diversity of frugivores. Despite supposed strong dispersal ability, as evidenced by their presence throughout the oceanic Philippines, the family is almost completely truncated by Wallace’s line: only a single genus, Thapsinillas, occurs in the Moluccas. The family is widespread throughout the Philippine archipelago—occurring even on very small and remote islands. The Philippines harbors 11 bulbul species that are placed in five genera. We follow the taxonomy of Fishpool and Tobias (2005) except for the taxonomic treatment of Iole palawanensis where we follow Dickinson (2003). Six species of bulbuls are endemic to the Philippines: five are endemic to oceanic islands of the Philippines (Pycnonotus urostictus, Ixos philippinus, Ixos rufigularis, Ixos everetti and Ixos siquijorensis) and one occurs only in the Palawan region (I. palawanensis). Four species are shared with the Sunda region, of which three are found in the Philippines only on Palawan (Pycononotus atriceps, Pycononotus plumosus, and Alophoixus bres) and the other is distributed throughout the oceanic Philippines (Pycnonotus goiavier) except the Batanes-Babuyan island chain (Fig. 1). The other non-endemic species, Microscelis amaurotis, occurs only on small islands in the Batanes-Babuyan island group north of Luzon and has a range that extends north through Taiwan and the Ryukyu archipelago to northern Japan and the Korean peninsula. Many of these species include multiple described subspecies and some workers have suggested that some of these races merit recognition as full species (Fishpool and Tobias, 2005, Allen, 2006, Peterson, 2006).
A recently published molecular phylogeny of bulbuls (Moyle and Marks, 2006) recovered two main lineages—one exclusively African and the other mostly Asian. Their study included only five Philippine species and all but one were widespread species sampled from localities outside of the Philippines. In the present study, we use the Moyle and Marks (2006) phylogenetic framework for bulbuls to examine the origin and diversification of Philippine members of the family. In particular, we address the following questions: (1) how many independent colonization events spawned the Philippine bulbul radiation? (2) do temporal patterns of colonization history suggest clustered dispersal events, potentially facilitated by specific historical factors, or random sweepstakes dispersal? (3) do genetic data reflect Palawan Island’s recent land connection to the islands of the Sunda Shelf? (4) what general patterns of colonization and diversification can be inferred from the genealogical history of the Philippines’ bulbul fauna?
Section snippets
Materials and methods
We used DNA sequence data for 28 species from Moyle and Marks’ (2006) study of bulbul systematics that used the following markers: the entire second and third subunits of mitochondrial nicotinamide adenine dinucleotide dehydrogenase (ND2 and ND3) and the seventh intron of the nuclear Beta-Fibrinogen (Fib7). This dataset was expanded by adding 46 individuals and sequencing an additional nuclear gene, the fifth intron of the Transforming Growth Factor β2 (TGF5), for all samples. In total, ingroup
Sequence attributes
The final dataset had a total alignment length of 2907 bp of combined DNA sequences from ND2, ND3, Fib7 and TGF5 (Table 3). We sequenced partial or entire genes for all samples except for the TGF5 intron of Pycnonotus montis and Iole olivacea 1. A total of 1118 characters (38%) were parsimony informative (Table 3). All sequences were deposited in GenBank (Accession Nos. GU112528–GU112737). Aligned ND2 and ND3 sequences contained no stop codons and appeared to be of mitochondrial origin.
Taxonomy
Proposing a complete taxonomic revision of Asian bulbuls is beyond the scope of this study but some changes in the taxonomy of Philippine bulbuls are mandated based on these data. Individuals from two species, Pycnonotus plumosus and I. philippinus, did not form clades. Monophyly of each of these two taxa was not rejected by an SH Test; however, this test is considered very conservative (Goldman et al., 2000, Buckley and Cunningham, 2002) and has a relatively low power of discrimination.
Biogeography
The inferred phylogenetic relationships of Philippine bulbuls suggest eight independent colonization events of the Philippine islands—one each by Pycnonotus atriceps, P. urostictus, P. plumosus cinereifrons, P. goiavier, A. bres frater, I. palawanensis, M. amaurotis and bulbuls of the genus Ixos. However this is not to say that the Philippine bulbul fauna was assembled only via colonization. We recovered a sizeable clade of bulbuls endemic to the Philippines that included a minimum of six
Acknowledgments
We are grateful to J. Reynon, N. Puna, J. Fernandez and R. Fernandez for assistance in the field, H. Shult for assistance in laboratory work, and J. Oaks and J. Essselstyn for assistance with using BEAST. We thank D. Willard and J. Bates (FMNH), R. Brumfield (LSUMNS), M. Lakim and J. Nais (Sabah Parks museum) and R. Corado (WFVZ) for specimen loans. J. Esselstyn, A. T. Peterson and two anonymous reviewers provided useful comments on the manuscript. We thank the Department of Environment and
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