Explosive avian radiations and multi-directional dispersal across Wallacea: Evidence from the Campephagidae and other Crown Corvida (Aves)

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Abstract

The systematic relationships among avian families within Crown Corvida have been poorly studied so far and as such been of limited use for biogeographic interpretations. The group has its origin in Australia and is thought to have colonized Africa and the New World via Asia beginning some 35 Mya when terranes of Australian origin approached Asian landmasses. Recent detailed tectonic mapping of the origin of land masses in the region around Wallace’s line have revealed a particularly complex movement of terranes over the last 20–30 Myr. Thus the biogeographic dispersal pattern of Crown Corvida is a particularly exciting case for linking vicariance and dispersal events with Earth history. Here we examine phylogenetic affinities among 72 taxa covering a broad range of genera in the basal radiations within Crown Corvida with an emphasis on Campephagidae and Pachycephalidae. Bayesian analyses of nuclear DNA sequence data identified the family Campephagidae as monophyletic but the large genus Coracina is not. Within the family Pachycephalidae the genera Pachycephala and Colluricincla are paraphyletic with respect to each other. The resulting phylogeny suggests that patterns of dispersal across Wallace’s line are complex and began at least 25 Mya. We find evidence of explosive radiations and multi-directional dispersal within the last 10 Myr, and three independent long distance ocean dispersal events between Wallacea and Africa at 10–15 Mya. Furthermore, the study reveals that in the Campephagidae a complex series of dispersal events rather than vicariance is the most likely explanation for the current biogeographic pattern in the region.

Introduction

The marked difference in fauna and flora between Asia and Australia has fascinated biologists for centuries. Alfred Russell Wallace was the first to make detailed accounts of these differences and the zoogeographical boundary between Asia and Australia known as Wallace’s line (Wallace, 1876). Wallace himself changed this boundary several times, in particular as Sulawesi contained fauna and flora belonging to both western and eastern regions. Today we know that major plates have collided in the Sulawesi area (Hall, 1998, Hall, 2002, Holloway, 1998, Moss and Wilson, 1998; Fig. 1) and it is no surprise that Wallace found it difficult to decide whether this island belonged to one region or the other. Another important aspect of the plate tectonics is that island arcs on the boundary towards the Pacific Ocean were squeezed between the advancing Australian/Papuan plate and the Ontong Java plateau in the Pacific, and moved rapidly to the west, just in front of New Guinea, creating opportunities for dispersal of birds within the archipelagos from Melanesia to the Philippines. Molecular phylogenies of several taxonomic groups (examples in Hall and Holloway, 1998, Barber et al., 2000) have been undertaken to elucidate biogeographic patterns within and across Wallacea. However, without robust phylogenies it has been very difficult to assess dispersal and differentiation patterns and the importance of vicariance linked with the movement of plate fragments within this region.

Based on analysis of protein allozymes, Christidis and Schodde (1991) suggested that the large oscine radiation (songbirds) originated in eastern Gondwana (proto-Australasia-Antarctica). There is now significant DNA sequence support for the view that the basal oscine lineages (Menuroidea and Meliphagoidea of Sibley and Ahlquist, 1990) originated in the Australo-Papuan region (and probably East Antarctica as well, considering the early Tertiary climate) (Barker et al., 2002, Ericson et al., 2002a, Ericson et al., 2002b) and radiated there, mostly as resident forest birds. These and other studies also indicate that more terminal groups, the Crown Corvida, dispersed out of Australia to other continents (Barker et al., 2002, Barker et al., 2004, Ericson et al., 2002a, Fuchs et al., 2006a, Jønsson and Fjeldså, 2006a) beginning 35 Mya. The basal clades within Crown Corvida are among the most understudied groups of passerine birds today (Jønsson and Fjeldså, 2006b). These include Campephagidae, Pachycephalidae, Oriolidae and Vireonidae. Apart from Vireonidae, these families are distributed mainly in Australia, Southeast Asia and Africa. Fuchs et al. (2007) developed a preliminary phylogenetic hypothesis for the Campephagidae (cuckoo-shrikes and allies) but focused on the biogeographic affinities of African and Indo-Malayan lineages. Consequently, many Wallacean and Australo-Papuan taxa were not examined. In the present study we focus on aspects of two assemblages that have large radiations within the Australo-Asian region: the geographically widespread family Campephagidae which comprises 6 genera and 87 species (Gill and Wright, 2006 disregarding the genus Hemipus see discussion further down) and the Australo-Papuan centered genus Pachycephala.

The aim of this study is: (1) to further establish relationships among and within the Crown Corvida assemblages, most notably Campephagidae and Pachycephalidae; (2) to provide a more detailed picture of the biogeographic and dispersal patterns of Crown Corvida across and within Wallacea supported by time estimates; and (3) to assess the relative roles of vicariance and dispersal in shaping oscine diversification in the region.

Section snippets

Taxon sampling and laboratory procedures

The lack of fresh tissue samples for DNA extraction has probably been the major reason that few studies have focused on these radiations so far. With careful primer design we have been able to obtain DNA sequences from old museum specimens (e.g. Irestedt et al., 2006) enabling us to obtain a broad taxon sampling of Campephagidae and Pachycephala. We also include several taxa whose affinities remain controversial e.g. Hylocitrea bonensis, Platylophus galericulatus, Colluricincla tenebrosa,

Results

The trees obtained from the Bayesian analyses of the individual genes were generally topologically congruent (Fig. 3, Fig. 4, Fig. 5); only three nodes, mostly terminals, were recovered as incongruent (congruence being supported by bootstrap values or posterior probabilities greater than 70% and 0.95, respectively). These nodes involve: (1) the relationships of P. solaris and P. ethologus within Pericrocotus, with G3PDH favouring solaris with cantonensis/divaricatus (PP = 0.96) whereas myoglobin

Discussion

Previous studies have confirmed an Australian/Papuan origin for the basal Crown Corvida radiation, including Campephagidae and Pachycephalidae (Barker et al., 2002, Ericson et al., 2002a, Ericson et al., 2002b, Fuchs et al., 2006a, Jønsson and Fjeldså, 2006b). The family Pachycephalidae is still mainly distributed within Australia/New Guinea and adjacent archipelagos. The Australo-Papuan centered Colluricincla harmonica, forms a deep branch in our phylogeny, in accordance with the

Acknowledgments

We are grateful to the following people and institutions for granting access to toe-pad, blood and tissue samples, Louisiana State University (LSU), Nate Rice and Leo Joseph (ANSP) Sharon Birks (UWBM), James Dean and Mike Braun (USNM), John Bates, Shannon Hackett and David Willard (FMNH), Mark Adams and Robert Prys-Jones (BMNH) and Giovanni Boano (MCSNC). Annie Tillier, Céline Bonillo and Josie Lambourdière (MNHN) provided invaluable help during laboratory work. Laboratory work at MNHN was

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