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Flycatchers (Terpsiphone

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Flycatchers (Terpsiphone Journal of Biogeography (J. Biogeogr.) (2012) 39, 1900–1918 ORIGINAL Dynamic colonization exchanges ARTICLE between continents and islands drive diversification in paradise-flycatchers (Terpsiphone, Monarchidae) Pierre-Henri Fabre1*, Martin Irestedt2, Jon Fjeldsa˚1, Rachel Bristol3, Jim J. Groombridge3, Mohammad Irham4 and Knud A. Jønsson1 1Center for Macroecology Evolution and ABSTRACT Climate at the Natural History Museum of Aim We use parametric biogeographical reconstruction based on an extensive Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen DNA sequence dataset to characterize the spatio-temporal pattern of colonization Ø, Denmark, 2Molecular Systematics of the Old World monarch flycatchers (Monarchidae). We then use this Laboratory, Swedish Museum of Natural framework to examine the role of dispersal and colonization in their evolutionary History, PO Box 50007, SE-104 05 Stockholm, diversification and to compare plumages between island and continental Sweden, 3Durrell Institute of Conservation and Terpsiphone species. Ecology, School of Anthropology and Location Africa, Asia and the Indian Ocean. Conservation, University of Kent, Canterbury CT2 7NR, UK, 4Research Center For Biology, Methods We generate a DNA sequence dataset of 2300 bp comprising one Cibinong Science Center (CSC), JL. Raya nuclear and three mitochondrial markers for 89% (17/19) of the Old World Jakarta – Bogor Km.46, Cibinong 16911, Monarchidae species and 70% of the Terpsiphone subspecies. By applying Bogor, Indonesia maximum likelihood and Bayesian phylogenetic methods and implementing a Bayesian molecular clock to provide a temporal framework, we reveal the evolutionary history of the group. Furthermore, we employ both Lagrange and Bayes-Lagrange analyses to assess ancestral areas at each node of the phylogeny. By combining the ancestral area reconstruction with information on plumage traits we are able to compare patterns of plumage evolution on islands and continents. Results We provide the first comprehensive molecular phylogenetic reconstruction for the Old World Monarchidae. Our phylogenetic results reveal a relatively recent diversification associated with several dispersal events within this group. Moreover, ancestral area analyses reveal an Asian origin of the Indian Ocean and African clades. Ancestral state reconstruction analyses of plumage characters provide an interpretation of the plumage differentiation on islands and continents. Ancestral plumage traits are inferred to be close to those of the Asian paradise-flycatcher (Terpsiphone paradisi), and island species display a high degree of plumage autapomorphy compared with continental species. Main conclusions Terpsiphone paradisi is polyphyletic and comprises populations that have retained the ancestral plumage of the widespread Terpsiphone genus. The genus appears to have colonized south-west Asia, the Indian Ocean and Africa from eastern Asia. The phylogeny and divergence time estimates indicate multiple simultaneous colonizations of the western Old World by Terpsiphone. These results reinforce a hypothesis of range expansions of a *Correspondence: Pierre-Henri Fabre, Center for Macroecology Evolution and Climate at the Terpsiphone paradisi-like ancestor into eastern Asia and the western Old World. Natural History Museum of Denmark, Keywords University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark. Africa, Asia, biogeography, colonization, dispersal, Indo-Pacific, island, Monar- E-mail: [email protected] chidae, plumage, speciation. 1900 http://wileyonlinelibrary.com/journal/jbi ª 2012 Blackwell Publishing Ltd doi:10.1111/j.1365-2699.2012.02744.x Colonization and diversification in paradise-flycatchers World Monarchidae, the genus Terpsiphone constitutes the INTRODUCTION clearest example of a dispersalist radiation, as evident from its Dispersal to, and colonization of, new land is widely accepted wide distribution and the occurrence of several distinct taxa on to be amongst the key drivers of speciation, and these processes remote islands. have contributed to the diversification of many organisms The genus Terpsiphone Gloger, 1827 (Old World paradise- (Simpson, 1953; Mayr, 1963). Indeed, these non-ecological flycatcher) comprises 13 extant species and is distributed mechanisms of divergence may have played a prominent role throughout the tropics of the Old World, including the in some of the most remarkable evolutionary and adaptive Philippines, the islands of the Indian Ocean and the Gulf of radiations (Rosenzweig, 1995; Groth, 1998; Moore & Don- Guinea (Fig. 1). The wide species distribution across a broad oghue, 2007, 2009; Grant & Grant, 2008; Losos, 2010; Jønsson range of mesic thicket and forest habitats make this genus an et al., 2011), and there is now considerable evidence that many excellent group for studying dispersal and speciation dynamics lineages that have successfully colonized new land have also between islands and continents. Given that the diversification undergone numerous speciation events (Steppan et al., 2004; within the Monarchidae took place mainly in the middle/late Moyle et al., 2009; Van Bocxlaer et al., 2010; Fritz et al., 2011; Miocene (Filardi & Moyle, 2005; Jønsson et al., 2011), Purvis et al., 2011). In these non-adaptive radiations, specia- vicariance can be reasonably dismissed as a factor contributing tion precedes ecological diversification, and geographical to speciation between Africa and Asia. Indian Ocean islands isolation by allo/parapatric barriers is the main factor under- and archipelagoes have not been connected to Africa or Asia in lying these speciation events (Rundell & Price, 2009). There- the last 50 million years (Myr). Therefore dispersal seems to be fore, geographical isolation on newly available land is likely to the only mechanism by which this island region could have be the principal driver of diversification in diverse groups been colonized. Indeed, recent biogeographical studies (see without ecological differentiation (e.g. Cameron et al., 1996; Warren et al., 2010) highlight a number of connections Comes et al., 2008; Phillimore & Price, 2008; Price, 2008). between Asian and Indian Ocean avifaunas. Speciation by geographical isolation appears to be particu- Among Asian Terpsiphone, several T. paradisi subspecies larly common amongst oscine passerine birds, for example in have spread across the entire Asian continent, and their many families within the Passerida (Price, 2008) and the core relationship with species in the Philippines, Palawan and Japan Corvoidea (Jønsson et al., 2011) radiations, in which large remains unknown. The geological history of Asia has been very numbers of similarly coloured species replace each other in dynamic and complex throughout the Cenozoic (Hall, 2002), different geographical regions. Within the core Corvoidea, and it is likely that the distribution and plumage variation of there are many examples (Fritz et al., 2011) where coloniza- Asian Terpsiphone was shaped by major historical vegetational tions of newly formed islands or archipelagos have led to a and climatic changes (Heaney, 1991; Bird et al., 2005; Patou substantial increase in species diversity, for instance the island et al., 2010). radiations of highly dispersive birds such as the Pachyceph- The large diversity of plumage phenotypes (Stresemann, alidae (Jønsson et al., 2010a), the Campephagidae (Jønsson 1924; Salomonsen, 1933a,b; Chapin, 1948) in the widely et al., 2010b) and the Monarchidae (Cibois et al., 2004; Filardi distributed continental species in Asia (the Asian paradise- & Moyle, 2005; Filardi & Smith, 2005). The core Corvoidea flycatcher) and Africa (the African and black-headed paradise- have recently been shown to have originated within an island flycatchers) presents a challenge to systematists, but some setting, and all members of this large radiation seem to be well common traits are evident. For example, all paradise-flycatch- adapted to persisting in archipelagos and to dispersing ers display sexual dimorphism (Mulder et al., 2002). Most of (Jønsson et al., 2011). Indeed, a number of studies of the core the members of Terpsiphone exhibit a crest, long central tail corvoid families have revealed complex colonization histories quills and rufous plumage. Five species lack long central tail for several families, reflecting their great abilities to disperse quills, and they all occur in the primary forests of Africa (most and to adapt within insular regions. Members of the Monar- of the T. rufiventer subspecies, T. bedfordi, T. batesi)oron chidae (90 species; Clements, 2007) belong to the corvid islands (T. cyanescens, T. bourbonnensis). Apart from two passerines (Barker et al., 2002). They are widely distributed Indian Ocean species (T. mutata, T. bourbonnensis), all island from the Old World to Australia and Oceania, and high species species display unicoloured plumages. This phenomenon is diversity is associated with a multitude of island allospecies also known from other avian island taxa (Mayr & Diamond, (Filardi & Smith, 2005; Uy et al., 2009) and even with 2001) and includes melanism (Theron et al., 2001; Uy et al., ‘upstream’ colonization, whereby the direction of dispersal is 2009; Driskell et al., 2010). One explanation for this might be from islands to the mainland (Filardi & Moyle, 2005; that rapid evolution after colonization and mutations linked Bellemain & Ricklefs, 2008; Cibois et al., 2011). The family with sexual selection or drift could account for the amount
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