A multilocus coalescent analysis of the speciational history of the Australo-Papuan butcherbirds and...

Molecular Phylogenetics and Evolution 66 (2013) 941–952

Contents lists available at SciVerse ScienceDirect

Molecular Phylogenetics and Evolution

journal homepage: www.elsevier .com/ locate /ympev

A multilocus coalescent analysis of the speciational history of the Australo-Papuanbutcherbirds and their allies

Anna M. Kearns a,c,⇑, Leo Joseph b, Lyn G. Cook a

a The University of Queensland, School of Biological Sciences, Brisbane, QLD 4072, Australiab Australian National Wildlife Collection, CSIRO Ecosystem Sciences, GPO Box 1700, Canberra, ACT 2601, Australiac Department of Biological Sciences, University of Maryland, Baltimore County, Baltimore, MD 21250, USA

a r t i c l e i n f o

Article history:Received 2 April 2012Revised 19 November 2012Accepted 23 November 2012Available online 5 December 2012

Keywords:AustraliaClimate changeCracticidaeIncomplete lineage sortingNew Guinea⁄BEAST

1055-7903/$ - see front matter � 2012 Elsevier Inc. Ahttp://dx.doi.org/10.1016/j.ympev.2012.11.020

⇑ Corresponding author at: The University of QueSciences, Brisbane, QLD 4072, Australia.

E-mail address: [email protected] (A.M. K

a b s t r a c t

Changes in geology, sea-level and climate are hypothesised to have been major driving processes of evo-lutionary diversification (speciation and extinction) in the Australo-Papuan region. Here we use completespecies-level sampling and multilocus (one mitochondrial gene, five nuclear loci) coalescent analyses toestimate evolutionary relationships and test hypotheses about the role of changes in climate and land-scape in the diversification of the Australo-Papuan butcherbirds and allies (Cracticinae: Cracticus, Stre-pera, Peltops). Multilocus species trees supported the current classification of the morphologically,ecologically and behaviourally divergent Australian Magpie (Cracticus tibicen (previously Gymnorhina tibi-cen)) as a member of an expanded genus Cracticus, which includes seven other species with ‘butcherbird’morphology and behaviour. Non-monophyly of currently recognised species within Peltops and thewhite-throated butcherbird species-group (C. argenteus, C. mentalis, C. torquatus) at both mtDNA andnuclear loci suggest that a comprehensive taxonomic revision is warranted for both of these groups.The time-calibrated multilocus species tree revealed an early divergence between the New Guinean rain-forest-restricted Peltops lineage and the largely open-habitat inhabiting Cracticus (butcherbirds and mag-pies) plus Strepera (currawongs) lineage around 17–28 Ma, as well as a relatively recent radiation oflineages within Cracticus over the past 8 Ma. Overall, patterns and timings of speciation were consistentwith the hypothesis that both the expansion of open sclerophyllous woodlands 25–30 Ma and the forma-tion of extensive grassland-dominated woodlands 6–8 Ma allowed the radiation of lineages adapted toopen woodland habitats.

� 2012 Elsevier Inc. All rights reserved.

1. Introduction

The Australo-Papuan region has experienced substantialclimatic and landscape change over the past 30 million years(Bowler, 1982; Kershaw et al., 1994; Veevers, 2000; Zachos,2001; Hall, 2002; Hope et al., 2004; Martin, 2006). Of particularsignificance was the onset and progressive aridification of theAustralian landmass, which by c. 2.6 Ma had established the dis-junction between open woodland- and desert-dominated Australiaand tropical rainforest-dominated New Guinea that persists today(Bowler, 1982; Kershaw et al., 1994; Martin, 2006). The progressivearidification of Australia can be divided into four major phases: (1)initial contraction of rainforests and expansion of open sclerophyl-lous habitats 25–30 Ma (Kershaw et al., 1994; Martin, 2006), (2)major onset of aridification and further expansion of open-habitats(temperate sclerophyll, tropical savanna, and arid grasslands)

ll rights reserved.

ensland, School of Biological

earns).

around 15 Ma (Zachos, 2001; Martin, 2006), (3) global expansionof C4-dominated savanna and other grassland-dominated habitatsaround 6–8 Ma (Cerling et al., 1997, 2011; Beerling and Osborne,2006), and (4) severe aridity, and frequent fluctuations betweenwarm-wet and cool-dry (arid) conditions during the Pleistoceneglacial cycles 11.7 kya – 2.6 Ma (Bowler, 1982; Martin, 2006;Williams et al., 2009). Concurrent with these climatic changeswere major changes in sea-level that caused the Arafura shelfbetween Australia and southern New Guinea to be intermittentlyexposed since the Miocene (Veevers, 2000; Chivas et al., 2001; Hall,2002; Naish et al., 2009), and geological changes that caused theaccretion of the proto-New Guinean islands and the uplift of thecentral ranges resulting in the formation of the current NewGuinean landmass around 2–5 Ma (Pigram and Davies, 1987;Veevers, 2000; Hall, 2002).

Diversification (speciation and extinction) of biota in Australiaand New Guinea is hypothesised to have been driven by complexinteractions between these changes in geology, sea-level and cli-mates via both stochastic processes such as extinction and geneticdrift following vicariance or dispersal, and ecological adaptation to

http://dx.doi.org/10.1016/j.ympev.2012.11.020

mailto:[email protected]


http://www.sciencedirect.com/science/journal/10557903

http://www.elsevier.com/locate/ympev

942 A.M. Kearns et al. / Molecular Phylogenetics and Evolution 66 (2013) 941–952

novel environmental conditions (Schodde and Calaby, 1972;Heinsohn and Hope, 2006; broader reviews in Byrne et al., 2008,2011; Bowman et al., 2010). Specifically, aridification on the Aus-tralian landmass over the past 25 Ma is expected to have openednew adaptive niches for arid-adapted lineages to exploit. It alsowould have caused range contractions, geographic isolation andextinction of lineages adapted to mesic-habitats (rainforest andother closed-canopy wet forests) in Australia (e.g. Byrne et al.,2008, 2011). Conversely, the long-term presence of large-standsof closed-canopy rainforest habitats in New Guinea and on the pro-to-New Guinean islands is hypothesised to have provided a majorrefuge for mesic-adapted lineages as aridity increased in Australia(Schodde and Calaby, 1972; Heinsohn and Hope, 2006; Schodde,2006).

Discriminating between the relative roles of specific climaticand geological events in promoting diversification requires theuse of an explicit hypothesis-based spatio-temporal framework(Knowles, 2009; Crisp et al., 2011). Recent attempts using time-cal-ibrated phylogenies have supported the hypothesis that increasingaridity from 25 Ma allowed the diversification of arid-adapted lin-eages in Australia (e.g. Crisp et al., 2004; Meredith et al., 2008; Fuj-ita et al., 2010; Pepper et al., 2011; Toon et al., 2012), and that theproto-New Guinean islands supported biota prior to the formationof the New Guinean landmass (Joseph et al., 2001, 2011; Krajewskiet al., 2004; Westerman et al., 2006; Roelants et al., 2007; Malekianet al., 2010; Macqueen et al., 2010; Jønsson et al., 2011; Toon et al.,2012). However, there are still too few studies incorporatingmultilocus datasets and complete sampling of extant taxa andkey geographic regions (e.g. New Guinea, central Australia andnorth-western Australia) to make robust inferences about the gen-erality of these hypotheses.

In this study we use a multilocus spatio-temporal frameworkand complete species-level sampling of the Australo-Papuanbutcherbirds and their relatives (Passeriformes: Corvoidea: Artam-idae: Cracticinae: Cracticus, Peltops, Strepera) to further testhypotheses about the influence of changes in climate and land-scape on the diversification of the biota of Australia and New Gui-nea. These birds are predominantly black and white predatorypasserines that exhibit a range of different habitat preferencesand ecological tolerances, and have a broad range of morphologicaladaptations to different foraging niches (Schodde and Mason,1999; Russell and Rowley, 2009). Strepera (Currawongs, three spe-cies) are large-bodied generalist scavengers that are endemic tothe temperate sclerophyll forests and woodlands of Australia. Pel-tops (Shieldbills, two species) are small-bodied aerial foragers thatare endemic to the highland and lowland rainforests of New Gui-nea. The eight currently recognized species of Cracticus occupyarid, temperate and rainforest habitats in Australia and New Gui-nea. Species of Cracticus (sensu Christidis and Boles, 2008) havetwo distinctive morphologies that are argued to represent morpho-logical adaptations to different foraging niches (see Schodde andMason, 1999) — short-legged, hooked-billed butcherbirds (sevenspecies), which are ‘perch-and-pounce’ predators, and the long-legged, pointed-billed Australian Magpie C. tibicen, which forageson the ground and probes in the soil for invertebrates. Based onmorphology, Cracticus has been further divided into four species-groups, and each has phenotypically differentiated forms in Aus-tralia and New Guinea: (1) the open-habitat generalist AustralianMagpie C. tibicen, which was previously placed in its own mono-typic genus Gymnorhina, (2) the rainforest and mangrove restrictedBlack Butcherbird C. quoyi, (3) the tropical savanna, temperate scle-rophyll and arid woodland-inhabiting ‘white-throated butcherbird’species-group (C. mentalis, C. argenteus, C. torquatus), and (4) the‘hooded butcherbird’ species-group, which has two species re-stricted to rainforests in New Guinea (C. cassicus, C. louisiadensis)

and one open-habitat generalist that is widespread in Australia(C. nigrogularis) (Schodde and Mason, 1999).

Phylogeographic studies of the Australian Magpie C. tibicen(Toon et al., 2007), the Pied Butcherbird C. nigrogularis (Kearnset al., 2010) and the Black Butcherbird C. quoyi (Kearns et al.,2011) have provided compelling evidence that cyclic aridity duringthe Pleistocene likely caused range contractions and vicarianceacross regions of unfavourably arid habitats in these species (seealso Byrne et al., 2008). Critically, however, the influence of earlierphases of aridity and changes in landscape have not been tested inthe Australo-Papuan butcherbirds and allies. Here we test whetherthe initial contraction of rainforests and expansion of open sclero-phyllous woodland habitats around 25–30 Ma (Kershaw et al.,1994; Martin, 2006) allowed the radiation of largely open-habitatinhabiting Strepera and Cracticus lineages, while the mesic-inhabit-ing Peltops lineage remained restricted to the tropical rainforests ofNew Guinea. This predicts that the Strepera plus Cracticus lineageshould not have radiated before extensive stands of open-habitatswere available —i.e. before the expansion of open sclerophylloushabitats in Australia 25–30 Ma. Secondly, we test whether theexpansion of savanna and other dry grassland-dominated openwoodlands 6–8 Ma (Cerling et al., 1997, 2011; Beerling and Os-borne, 2006; Martin, 2006) allowed the radiation of open wood-land inhabiting lineages within Cracticus. This predicts thatlineages with species that inhabit monsoon savanna and arid,semi-arid and temperate open-woodlands (i.e. C. tibicen, C. nigrog-ularis, white-throated species group: C. argenteus, C. mentalis, C.torquatus) should not have originated before the estimated timingof the expansion of extensive stands of these habitats 6–8 Ma (Cer-ling et al., 1997, 2011; Beerling and Osborne, 2006; Martin, 2006).

The secondary objective of this study is to estimate relation-ships among the Australo-Papuan butcherbirds and their allies,and to test morphology-based species boundaries within the spec-iose genus of butcherbirds, Cracticus. Artamidae is currently di-vided into two sub-families: the Australo-Papuan cracticines(Cracticinae: Strepera, Peltops, Cracticus) and the Australasianwoodswallows (Artaminae: Artamus) (Schodde and Mason, 1999;Christidis and Boles, 2008) — these sub-families have, at times,been considered separate families (Amadon, 1951; Russell andRowley, 2009). Despite recent interest in the evolution and rela-tionships of members of the Corvoidea, the relationships of theAustralo-Papuan butcherbirds and allies to other shrike-like andcrow-like birds are still a matter of debate (Yamagishi et al.,2001; Ericson et al., 2002; Barker et al., 2004; Fuchs et al., 2004,2006, 2012; Beresford et al., 2005; Fjeldså et al., 2006; Moyleet al., 2006; Manegold, 2008; Norman et al., 2009; Jønsson et al.,2011). Recent molecular studies provide support for a close rela-tionship between the Australo-Papuan cracticines, the Australasianwoodswallows (Artamus), Australo-Papuan Boatbills (Mach-aerirhynchus), Asian Ioras (Aegithinidae), the Bornean Bristlehead(Pityriasis gymnocehala), and African bush-shrikes (Malaconotidae),vangas (Vangidae) and helmet-shrikes (Prionopidae) (e.g. Fuchset al., 2006, 2012; Moyle et al., 2006; Norman et al., 2009; Jønssonet al., 2011), rather than the Old-World shrikes (Laniidae), Crows(Corvidae) or monarch-flycatchers (Monarchidae) with which theywere previously circumscribed (reviewed in Russell and Rowley,2009).

Critically, no study to date has had the taxonomic sampling nec-essary to (1) resolve the relationships within or among Peltops,Cracticus and Strepera, or (2) test the controversial decision ofChristidis and Boles (2008) (but see Storr, 1952) to place the mor-phologically distinct Australian Magpie C. tibicen within Cracticusrather than keeping it in monotypic Gymnorhina as proposed bySchodde and Mason (1999) on the basis of its strikingly differentmorphology and social behaviour. Within Cracticus, multilocus

A.M. Kearns et al. / Molecular Phylogenetics and Evolution 66 (2013) 941–952 943

phylogeographic studies suggest that New Guinean and Australianlineages of the Black Butcherbird (C. quoyi) might warrant speciesstatus (Kearns et al., 2011). However, there has been no moleculartest of relationships or species boundaries within either thehooded butcherbird species-group or the white-throated butcher-bird species-group despite debate surrounding (1) the recognitionof the melanistic Tagula Butcherbird, C. louisiadensis, as a memberof the hooded species-group (Amadon, 1951), and (2) the species-status of the north-western Australian Silver-backed Butcherbird C.argenteus, which is often argued to be a subspecies of the southernAustralian Grey Butcherbird C. torquatus (Amadon, 1951; Ford,1979; Schodde and Mason, 1999; Christidis and Boles, 2008).

2. Materials and methods

2.1. Molecular sampling

Sampling for each species was as follows: Cracticus argenteus(n = 32), C. torquatus (n = 36), C. mentalis (n = 13), C. cassicus(n = 6), C. louisiadensis (n = 2), C. nigrogularis (n = 14), C. quoyi(n = 38), C. tibicen (n = 6), Peltops blainvilli (n = 4), P. montanus(n = 3), Strepera fuliginosa (n = 1), S. versicolor (n = 1), and S. graculi-na (n = 1) (see Table A.1 in Appendix A for further details). Artamusleucorynchus was included as an outgroup for multilocus analyses(Table A.1). Sequences of representatives of putative sister lineagesof Artamidae (Malaconotidae, Platysteiridae, Vangidae, Aegithinaand Machaerirhynchus) (Barker et al., 2004; Fuchs et al., 2006), aswell as representatives of Artamus (see Table A.1), were includedfrom GenBank for the mtDNA locus.

DNA extractions from frozen tissue used a salt-based extractionmethod (Nicholls et al., 2000; Kearns et al., 2010). DNA was ex-tracted from toe-pads using a DNeasy Tissue Kit (Qiagen, Valencia,CA) with modifications to the manufacturers’ protocol to improveyield and to better maintain sterile conditions (for detailed descrip-tion of protocol see Kearns et al., 2011). One coding mitochondrialgene (NADH dehydrogenase subunit 2, ND2), and five non-codingnuclear introns (BRM-15, CHDZ-18, BF-7, GAPDH-11 and ODC-6&7) were analysed in this study (see Table A.2 in Appendix A forprimer details). PCR amplification followed the protocol describedin Kearns et al. (2011) — 1.5 lL MgCl2 (50 lM), 5 lL 5 � buffer,2 lL dNTPs (2 lM), 0.5 lL each primer (10 lM), 0.2 lL MangoTaqand template DNA (see Table A.2) and the following thermocyclerconditions: 94 �C for 4 min, 35 cycles of 94 �C for 30 s, 55 �C for30 s (1 min for ND2a fragment), 72 �C for 1 min and 72 �C for3 min. Only BRM-15 and ND2 were amplified and sequenced fortoe-pad specimens. We used ExoSAP to purify PCR product for alltoe-pad specimens, and some PCR products were purified usingammonium acetate (7.5 M) precipitation. All loci were sequencedcommercially (Macrogen, Seoul, South Korea) with the same prim-ers used for PCR amplification. CodonCode Aligner 3.0.1 (CodonCodeCorporation 2002–2009) was used to edit and align sequences. DNAsequences for some species are from previous phylogeographic-le-vel studies within Cracticus (Kearns et al., 2010, 2011).

The genotype of individuals with length polymorphisms wasdetermined using the ‘subtraction method’, which uses the shiftedpeak locations in the chromatogram of the forward and reverse se-quences to infer the individual alleles of heterozygous regions(Dolman and Moritz, 2006). PHASE v2.1 (Stephens and Donnelly,2003) was used to infer the genotype of individuals with multipleheterozygous sites statistically from 5 (BRM-15, CHDZ-18, BF-7) or10 (GAPDH-11, ODC-6&7) independent runs and using a phaseprobability threshold of 70% (Stephens and Donnelly, 2003). Het-erozygous sites with uncertain phase (<70%) were coded using IU-PAC codes, and kept in all downstream analyses except for networkinference. Indels were excluded from all analyses except for net-

work inference. Intra-locus recombination can seriously misleadphylogenetic inference if not properly accounted for (Martinet al., 2011). We therefore used the difference of sums-of-squares(DSS) method implemented in TOPALi v1 (Milne et al., 2004) tosearch for signals of recombination (significant DSS peaks) usinga 100 bp sliding window and a 10 bp step size. Significant evidenceof recombination was found in BF-7, and as such, all analyses usethe last 402 bp of this locus that showed no evidence of recombi-nation. All sequences were deposited in GenBank (KC162242-KC162825; see Table A.1 in Supplementary material).

2.2. Single-locus genealogies

The mtDNA phylogeny was estimated using maximum likeli-hood (implemented in RAxML v7.0.4; Stamatakis, 2006) and Bayes-ian inference (implemented in MrBayes 3.1.2; Huelsenbeck andRonquist, 2001) with codon positions treated as different partitionsand each with a GTR+I+G substitution model. Maximum-likelihoodused the ‘fast ML’ algorithm, and 1000 bootstrap pseudoreplicatesto evaluate topological support. Two Bayesian MCMC runs wererun for 14 million generations using default heat values. Conver-gence and mixing was assessed by ensuring that split frequencieswere below 0.01, that posterior density plots from independentruns did not show obvious trends and that the harmonic meansfrom independent runs did not differ by more than 3. A burnin of10 million generations was excluded from each run on the basisof these criteria. Given that there is some controversy about theplacement of C. tibicen as sister to, or nested among, the other spe-cies of Cracticus, we calculated Bayes Factors (BF; Kass and Raftery,1995; Nylander et al., 2004) to discriminate between the two alter-native hypotheses most often considered in prior literature (cfSchodde and Mason, 1999; Christidis and Boles, 2008; Russelland Rowley, 2009): (1) C. quoyi and C. tibicen form a monophyleticclade (estimated tree), and (2) C. tibicen is the sister to all otherCracticus species (constrained tree). The constrained Bayesian anal-ysis followed identical settings as the unconstrained analysis ex-cept that the monophyly of Cracticus species with ‘butcherbird’morphology was enforced (Cracticus sensu stricto: Schodde and Ma-son, 1999). Convergence and mixing was assessed following theabove criteria and a burnin of 1.26 million generations was ex-cluded. Harmonic means of the marginal likelihoods from the con-strained and unconstrained runs were used to calculate BayesFactors (BF) using the threshold value of 2log10BF = 10 as evidenceagainst the alternative hypothesis (Kass and Raftery, 1995;Nylander et al., 2004).

For the five nuclear loci, unrooted allele networks are presentedrather than rooted phylogenies owing to low polymorphism andincomplete lineage sorting within each genus (see Results).Unrooted allele networks were estimated in TCS 1.21 (Clementet al., 2000) using the statistical parsimony method and a 95% con-nection limit. For all nuclear loci except GAPDH, indels were codedas presence or absence characters and included in network infer-ence (multi-nucleotide indels were considered to result from a sin-gle insertion-deletion event).

2.3. Species tree estimation and divergence dating

The multispecies coalescent ⁄BEAST algorithm (implemented inBEAST v1.6.1; Drummond and Rambaut, 2007; Heled and Drum-mond, 2010) was used to estimate a species tree from the five nu-clear loci alone, and the mtDNA and nuclear loci combined.Morphology-based species delineations sensu Christidis and Boles(2008) were used as a priori ‘species boundaries’ in the ⁄BEASTanalysis with the exception of Peltops, C. quoyi, C. argenteus andC. torquatus. For Peltops, mtDNA and nuclear loci sequenced in thisstudy were incongruent with the morphology-based species


boundaries within Peltops but two genetic groups were consis-tently identified across all six loci. This suggested that paraphylyin Peltops likely results from incorrect taxonomy rather thanincomplete lineage sorting (see Results). We therefore treatedthe two genetic groups as ‘species’ in ⁄BEAST analyses (‘Peltopsclade1’ and ‘Peltops clade2’). For C. quoyi, the New Guinean andAustralian lineages were treated as separate species for the pur-poses of the ⁄BEAST analysis on the basis of Kearns et al.’s (2011)findings of significant differentiation of these lineages at bothmtDNA and nuclear loci. Cracticus argenteus was defined as an apriori species in the ⁄BEAST analyses (sensu Schodde and Mason,1999) rather than as a subspecies of C. torquatus (sensu Christidisand Boles, 2008) given mtDNA and nuclear differentiation thatwas consistent with species-level divergence of these two forms(see Results; A. Kearns, L. Joseph, L. Cook unpublished). Owing tomissing nuclear data (see Table A.1), C. louisiadensis was omittedfrom the ⁄BEAST analyses. ⁄BEAST can handle different numbersof individuals for different loci therefore all sampled sequencesfor each locus were included in the analysis (see Table A.1) withone exception — C. argenteus mtDNA haplotypes nested within C.torquatus (see Results) were excluded from the combined mtDNAand nuclear ⁄BEAST analysis on the basis of analyses that stronglysuggest that this mtDNA haplotype lineage is introgressed from C.torquatus (A. Kearns, L. Joseph, L. Cook unpublished). This approachwas necessary as the inclusion of both paraphyletic mtDNA lin-eages sampled from C. argenteus in the ⁄BEAST analyses would biascoalescent time estimates for the white-throated species-group.⁄BEAST analyses used a Yule prior on the species tree. Substitu-

tion models for nuclear loci were selected in MrModeltest 2.2(Nylander, 2004) under the Akaike information criterion (AIC) —BRM-15: GTR+G, CHDZ-18: HKY+G, BF-7: HKY+G, ODC-6&7:HKY+I, GAPDH-11: HKY+I. Preliminary runs using a relaxed uncor-related lognormal clock for each locus were used to evaluatewhether a strict clock was applicable to the data. Posterior distri-butions of the substitution rate parameter of each nuclear locus in-cluded zero so we applied a strict clock to the nuclear loci insubsequent analyses. A relaxed uncorrelated lognormal clock wasused for the mtDNA locus. In the absence of a reliably estimatedsubstitution rate for the nuclear loci, and fossils available for nodecalibrations within the core Corvoidea, divergence dating was per-formed only for the combined mtDNA and nuclear dataset. Weused the robust fossil-calibrated estimate of average avian mtDNAsubstitution rate of 2.1% ± 0.1%/Ma (0.0105 ± 0.0005 substitution/site/lineage/Ma) (Weir and Schluter, 2008), which represents anaverage rate estimated across 12 avian orders within a time-framethat is relevant for this study. The substitution rate was appliedusing a normal distribution on the ucld.mean parameter for themtDNA locus. The nuclear-only analysis was run twice for4 � 108 generations (sampling every 5000 generations), and thecombined mtDNA and nuclear analysis was run twice for 1 � 109

generations (sampling every 5000 generations). We assessed con-vergence and calculated the appropriate burnin using ESS values(>200) and trends in the posterior distribution of each parameterin TRACER (v1.5; Rambaut and Drummond, 2007). In both analy-ses, the two independent runs were combined using LOGCOMBIN-ER (v1.6.1; Drummond and Rambaut, 2007) after excluding a 10%burnin from each run, and then a maximum-clade-credibility treewas calculated using TREEANNOTATOR (v1.6.1; Drummond andRambaut, 2007).

3. Results

The mtDNA dataset consisted of 1017 bp, although only the first653 bp could be obtained from toe-pads of museum specimens(Table A.1). No indels or premature stop codons were observed in

the mtDNA dataset. The nuclear introns had fewer phylogeneticinformative sites than the mtDNA locus: ND2 742/1017 bp, BF-7124/424 bp, BRM 62/335 bp, CHD 108/281 bp, GAPDH 45/296 bp,ODC 86/666 bp (number of phylogenetic informative sites/totalnumber of sites at each locus). The five nuclear loci contained be-tween 2 and 5 indels. Several indels were fixed within species andwithin genera. GAPDH contained a variable-length insertion-dele-tion multi-nucleotide repeat pattern that was found only amongmembers of the white-throated butcherbird group. This regionwas not included in analyses owing to ambiguity in the alignment.

3.1. Single-locus genealogies

The monophyly of each genus in Artamidae was strongly sup-ported (1.0/100; Bayesian posterior probability support/ML boot-strap support), however, there was no support for the monophylyof Artamidae sens. lat. (Schodde and Mason, 1999; Christidis andBoles, 2008). Peltops, Strepera and Cracticus (Cracticinae sensuSchodde and Mason, 1999; Christidis and Boles, 2008) formed aclade (0.97/83), which was sister to a clade comprising the Afri-can-centred bush-shrikes and allies (Malacontidae, Vangidae, andPlatysteiridae) (0.96/62). Artamus was the sister of this group(0.96/49), and Aegithina was sister to Artamus, though with littleor no support (0.85/47). Relationships within Strepera had no statis-tical support but our sampling was not designed to test this (Fig. 1).Maximum-likelihood placed S. versicolor and S. fuliginosa as sistershowever with no bootstrap support (45), while Bayesian analysesplaced S. versicolor and S. graculina as sisters (0.79). Samples identi-fied as Peltops blainvilli and P. montanus were not reciprocallymonophyletic and, instead, there was strong support for two geo-graphically overlapping clades (1.0/100 and 0.98/82, respectively)(Figs. 1 and 2b).

The mtDNA gene tree did not offer strong support for the phylo-genetic placement of C. tibicen. Cracticus tibicen and C. quoyi wereeach other’s sister in the 50% majority rule consensus tree, however,there was no statistical support for this relationship (0.74/51).There was also no support for the monophyly of C. quoyi (0.71/54). There was, however, strong support for the reciprocal mono-phyly of Australian (1.0/99) and New Guinean (1.0/99) lineages ofC. quoyi with respect to each other. The topology inferred by themtDNA gene tree is thus a four-way polytomy at the base of Cracti-cus consisting of the (1) white-throated + hooded lineage (1.0/100),(2) C. tibicen lineage, (3) New Guinea C. quoyi lineage, and (4) Aus-tralian C. quoyi lineage. Bayes Factors supported a significant differ-ence between the estimated phylogeny that placed C. tibicen and C.quoyi (0.74/51) as sisters and the alternative hypothesis that C. tibi-cen is sister to the rest of Cracticus sensu Schodde and Mason (1999)(monophyly not enforced: harmonic mean = -16416.01; mono-phyly enforced: harmonic mean = -16410.48; 2log10BF = 11.06).

Within the ‘white-throated + hooded’ lineage, there was no sta-tistical support for the reciprocal monophyly of the hooded species-group (C. louisiadensis, C. cassicus and C. nigrogularis) (0.81/79), butthere was strong support for the monophyly of the white-throatedspecies-group (C. argenteus, C. mentalis and C. torquatus) (1.0/100).The sister-relationship of the island endemic C. louisiadensis andNew Guinean C. cassicus was strongly supported (1.0/96). This is de-spite similarities in plumage that pied-plumaged C. cassicus and C.nigrogularis share to the exclusion of the more melanistic C. louis-iadensis. Critically, the mtDNA dataset did not provide support forspecies boundaries within the white-throated butcherbird speciesgroup as per the morphology-based taxonomic treatments ofSchodde and Mason (1999) (three species: C. argenteus, C. mentalis,C. torquatus) or Christidis and Boles (2008) (two species: C. mentalis,C. torquatus/argenteus). Instead, white-throated butcherbirdmtDNA haplotypes formed two reciprocally monophyletic clades(Fig. 1) — the first clade contained haplotypes from both C.

Fig. 1. Bayesian estimate of relationships among the Australo-Papuan butcherbirds and allies inferred by the mitochondrial gene ND2. Relationships are depicted by a fifty-percentage majority rule consensus rule tree. Bayesian posterior probability (above) and maximum-likelihood bootstrap support (below) values are indicated on severalnodes with conflicting or low support between methods. Branches are colour coded within Cracticus according to morphology-based species-boundaries (see Fig. 3 for thegeographic range of each species).


Fig. 2. Unrooted phased allele networks of five nuclear loci for (a) Cracticus, (b) Peltops and (c) Strepera. Small black circles represent unsampled haplotypes. For eachhaplotype the proportion of alleles sampled from each species follows the legend on the left. The map of New Guinea shows the geographic range of Peltops (modified fromRussell and Rowley, 2009) and the sampling localities of the four P. blainvilli and three P. montanus specimens included in this study.


argenteus and C. mentalis (1.0/100), and the second clade containedhaplotypes from C. argenteus and C. torquatus (1.0/98).

Despite low levels of variation and incomplete lineage sorting,the overall pattern of genetic variation within each nuclear locuswas consistent with most of the relationships and species bound-aries supported by the mtDNA gene tree (Figs. 1 and 2). Key simi-larities between the mtDNA and nuclear genealogies withinCracticus include the (1) close association of hooded and white-throated species-groups, (2) lack of sharing of alleles between C.tibicen and C. quoyi, and between C. cassicus, C. nigrogularis and C.louisiadensis and also between the hooded and white-throatedgroups, (3) differentiation of Australian and New Guinean lineagesof C. quoyi, and (4) non-reciprocal monophyly of white-throatedbutcherbird species regardless of their species limits under boththe 2-species (Schodde and Mason, 1999) or 3-species (Christidisand Boles, 2008) taxonomic treatments. Despite widespread shar-

ing of nuclear alleles, the three white-throated butcherbird speciesexhibit patterns of low to moderate differentiation at four of thefive nuclear loci (Fig. 2a: BF-7, BRM-15, GAPDH-11, ODC-6&7). Nu-clear loci are also broadly consistent with the differentiation of thetwo mtDNA clades within Peltops. Peltops blainvilli samples Pb1 andPb4 share alleles with P. montanus only at BF-7, whereas the othertwo P. blainvilli samples (Pb2 and Pb3) were consistently more clo-sely related to the three sampled individuals of P. montanus (Pm5,Pm6, Pm7) at each sampled locus than they were to individualsPb1 and Pb4 of P. blainvilli (Fig. 2b).

3.2. Multilocus species trees and divergence dating

Relationships among the Australo-Papuan cracticines inferredby ⁄BEAST using nuclear loci alone offered strong support for themonophyly of all three genera (Peltops, Strepera, and Cracticus),


the white-throated and hooded species-groups within Cracticus,and C. quoyi (Australian and New Guinean lineages are stronglysupported as each other’s sister pp = 1.0). There was support forthe sister relationship of Strepera and Cracticus (1.0), C. tibicenand C. quoyi (0.83) and hooded and white-throated species-groups(1.0) (Fig. 3). Combined coalescent analysis of the mtDNA and nu-clear loci produced a well-supported species tree that mirrored therelationships estimated from the nuclear loci alone with the excep-tion of relationships within Strepera — S. graculina and S. versicolorwere supported as sisters with moderate support (0.87) (Fig. 3).Only two nodes had posterior probability support below 0.95 —C. argenteus plus C. torquatus, and S. versicolor plus S. graculina(Fig. 3).

The timing of divergence between the lineage leading to thecracticine clade (Strepera, Cracticus, Peltops) and that leading to Art-amus (Fig. 3: 21–36 Ma; 95% HPD intervals) was broadly consistentwith the range of estimates derived for this node in several otherstudies using a range of different calibration techniques (fossiland biogeographic calibrations), different nuclear loci and differenttaxonomic sampling (e.g. 25.1–36.3 Ma, Fuchs et al., 2006; 20–27.7 Ma, Jønsson et al., 2010; 20–30 Ma, Jønsson et al., 2011).The split between rainforest-inhabiting Peltops lineage and theancestor of largely open-habitat inhabiting Strepera plus Cracticuslineage is estimated to have occurred around 16.9–28.3 Ma(Fig. 3). Strepera and Cracticus are estimated to have divergedaround 9.8–17.3 Ma in the mid-Miocene (Fig. 3). The two majorlineages within Cracticus (C. tibicen + C. quoyi lineage and hoo-ded + white-throated lineage) are estimated to have divergedaround 4.2–8.3 Ma, during the late Miocene to early Pliocene.

Fig. 3. Time-calibrated multilocus species tree for the Australo-Papuan cracticines. ChronmtDNA and nuclear intron ⁄BEAST analysis. Support values on nodes represent the poster(⁄in the nuclear only analysis S. graculina and S. fuliginosa were supported as sisters wiestimates of each node are provided. Vertical grey lines indicate the predicted timing oDistribution of present-day habitats in Australia and New Guinea (modified from Schoddand Rowley, 2009) and phenotypic variation within Peltops, Strepera and Cracticus.

Divergences between species of Cracticus occurred during the latePliocene and throughout the Pleistocene (110,000 ya – 5.8 Ma).The divergence of C. tibicen and C. quoyi is the oldest estimated spe-cies-level divergence within Cracticus having occurred within thePliocene (3.0–5.8 Ma). The youngest species-level divergences arein the late Pleistocene between the white-throated butcherbirdspecies (110,000–380,000 ya) (Fig. 3).

4. Discussion

Traditional phylogenetic approaches, which typically rely on asingle-locus or concatenation of multiple loci, do not account forgene tree discordance resulting from stochasticity in coalescenceand mutation rates across loci. Those methods typically often over-estimate divergence times and can provide misleading support fora phylogeny that does not track the true history of populationdivergence (Edwards and Beerli, 2000; Maddison and Knowles,2006; Carstens and Knowles, 2007; Edwards et al., 2007; Heledand Drummond, 2010; McCormack et al., 2010). By accountingfor the slow rate of mutation of non-coding nuclear introns andstochasticity in the lineage sorting process, coalescent methodsare better able to estimate the pattern and timing of speciationevents, and to delimit species boundaries despite widespread shar-ing of alleles (Maddison and Knowles, 2006; Carstens and Knowles,2007). In this study we exploited the newly developed multispe-cies coalescent model (⁄BEAST; Heled and Drummond, 2010) inorder to simultaneously estimate a robust species tree and diver-gence times for the Australo-Papuan cracticines (Fig. 3). Thispotentially more accurate estimation of the pattern and timing of

ogram represents the maximum-clade-credibility tree obtained from the combinedior probability support for the combined (above) and nuclear only (below) analyses

th low support (0.42)). The 95% highest posterior intervals on the divergence timef major phases of aridity in the Australo-Papuan region over the past 30 mya. (a)e, 1989). (b) Geographic ranges (modified from Schodde and Mason, 1999; Russell


speciation events within the Australo-Papuan cracticines allowedus to test diversification hypotheses and to estimate evolutionaryrelationships despite the presence of incomplete lineage sortingand overall lack of resolution in nuclear introns (Fig. 2).

4.1. Systematic relationships

As with previous studies (Fuchs et al., 2004, 2006, 2012; Yamag-ishi et al., 2001; Ericson et al., 2002; Barker et al., 2004; Beresfordet al., 2005; Moyle et al., 2006; Norman et al., 2009; Jønsson et al.,2011), our mtDNA phylogeny failed to robustly resolve the system-atic relationships within the Southern Hemisphere-centred radia-tion of shrike-like passerines (Australo-Papuan cracticines, theAustralasian woodswallows (Artamus), the African-centred mala-conotids and allies, the Asian Ioras (Aegithina) and the Australo-Papuan Boatbills (Machaerirhynchus)) (Fig. 1). Bayesian analysisof ND2 sequences showed no support for the Artaminae (Artamus)and the Cracticinae (Peltops, Strepera, Cracticus) as each other’sclosest relatives, thus Artamidae as currently circumscribed (sensuSchodde and Mason, 1999; Christidis and Boles, 2008) is not mono-phyletic in our analysis (Fig. 1). The lack of robust support for themonophyly of Artamidae sens lat. suggests that Cracticidae (Peltops,Strepera, Cracticus) and Artamidae (Artamus) could be reinstated asseparate families sensu Amadon, 1951 (see also Russell and Row-ley, 2009). However, accurate estimation of the history of diver-gence and taxonomy of this diverse radiation of shrike-likepasserines will require further work using increased locus and tax-on-sampling within the context of a rigorous multilocus coalescentspecies tree approach.

Multilocus species trees (combined nuclear and mtDNA, andnuclear only) were concordant with the morphology-basedhypotheses for the relationships among cracticine genera (Ama-don, 1951; Ford, 1979; Schodde and Mason, 1999; Higgins et al.,2006; Christidis and Boles, 2008; Russell and Rowley, 2009) —i.e. strong support for Strepera as the sister of Cracticus (com-bined/nuclear only: 1.0/1.0), and for the placement of the NewGuinean Peltops as the sister of (Strepera + Cracticus) (combined/nuclear only: 0.99/1.0) (Fig. 3). This accords with the circumscrip-tion of Peltops within the Cracticinae rather than with the Austral-asian woodswallows (Artaminae: Artamus) or the monarch-flycatchers (Monarchidae), as has been previously hypothesised(see references in Russell and Rowley, 2009; Norman et al., 2009;Jønsson et al., 2011).

Species-level discordance between gene trees and morphologywas observed within Cracticus, Peltops and Strepera (Figs. 1–3).However, our limited sampling of individuals and populationswithin Strepera do not permit supported statements about rela-tionships within and among the three species beyond offering evi-dence for the reciprocal monophyly of the genus (Figs. 1, 2c, and 3;Table A.1). Peltops showed a complex paraphyletic pattern delin-eating two geographically overlapping genetic groups that werenot consistent with morphology-based species boundaries (Figs. 1and 2). Our limited sample size precludes a formal taxonomic revi-sion of Peltops. However, based on our preliminary genetic dataand reports of complex patterns of plumage variation that do notdiscretely match current species boundaries (Russell and Rowley,2009), a comprehensive revision of phenotypic and genetic varia-tion in Peltops is warranted. The estimated time to most recentcommon ancestor of the two genetic groups within Peltops was1.8–4.6 Ma (Fig. 3), consistent with similar complex phylogeo-graphic patterns and deep divergences in other New Guinean spe-cies (e.g. macropods, genus Thylogale, Macqueen et al., 2010; birds,Colluricincla megarhyncha, Deiner et al., 2011).

Our analyses revealed two major findings that were inconsis-tent with morphology-based taxonomic expectations for relation-ships within Cracticus (Figs. 1–3) — the mtDNA paraphyly of C.

argenteus, and the placement of C. tibicen sister to C. quoyi ratherthan sister to all of the Cracticus species with ‘butcherbird’ mor-phology. Major conflict between mtDNA, nuclear introns and mor-phology within the white-throated butcherbird species-group(Figs. 1–3) could originate from (1) incorrect taxonomy: C. argen-teus is a cryptic species of two or more lineages, (2) mtDNA intro-gression between C. argenteus and either C. torquatus or C. mentalis,or (3) incomplete lineage sorting. We examine these alternativehypotheses elsewhere using increased taxon and locus sampling,and multilocus coalescent tests of divergence and gene flow (A.Kearns, L. Joseph, L. Cook unpublished).

Multilocus multispecies coalescent analyses provided strongsupport for the placement of C. tibicen sister to C. quoyi (Fig. 3), de-spite the lack of support for this relationship in the mtDNA genetree (Fig. 1). The placement of the morphologically, ecologicallyand behaviourally divergent C. tibicen as the sister of the BlackButcherbird C. quoyi to the exclusion of all other butcherbirdspecies is intriguing given that it is inconsistent with the morphol-ogy-based expectation that species with ‘butcherbird’ morpholo-gies should form a reciprocally monophyletic group. However,there are many similar examples where striking phenotypic differ-ences among closely related species have been hypothesised to re-sult from strong selective pressures on ecological traits that drivephenotypic adaptation to novel environments or ecological re-sources (e.g. Darwin’s finches, Sato et al., 1999; Australo-Papuanchowchillas and logrunners Orthonyx spp, Joseph et al., 2001; Mad-agascan Vangidae, Yamagishi et al., 2001; Reddy et al., 2012; NewWorld Crossbills, Parchman et al., 2006). A similar ‘ecological adap-tation’ hypothesis has been applied for the evolution of morpho-logical adaptations to an open terrestrial foraging niche in C.tibicen (Schodde and Mason, 1999; Higgins et al., 2006; Christidisand Boles, 2008; Russell and Rowley, 2009).

Irrespective of whether C. tibicen is sister to the rest of Cracticus,to a monophyletic C. quoyi, or to either the Australian or New Guin-ean lineages of C. quoyi, our findings provide strong evidence thatthe synonymy of Gymnorhina G.R. Gray, 1840 with Cracticus Vieil-lot, 1816 is valid, as advocated by Christidis and Boles (2008) andStorr (1952). A monophyly-based alternative of retaining Gym-norhina would require alternative taxonomic treatments such thatCracticus sens. strict. be split into either two, three or four genera.Although genus-group names are available for each (MelloriaMathews, 1912 for C. quoyi; Bulestes Cabanis, 1850 for the white-throated species-group (C. torquatus, C. argenteus, C. mentalis);and Cracticus Vieillot, 1816 for the hooded species-group (C. nigrog-ularis, C. louisiadensis, C. cassicus)), we consider such a splitting ap-proach is not warranted.

4.2. Biogeography

4.2.1. Changes in climate: aridification over the past 30 million yearsThe mostly open-habitat-inhabiting (Strepera + Cracticus) line-

age and the mesic-inhabiting Peltops lineage were estimated tohave diverged around 17–28 Ma during the mid-Oligocene/mid-Miocene (Fig. 3). This is consistent with the predictions of our firsthypothesis that open-habitat inhabiting lineages should not haveoriginated before the initial expansion of open sclerophyllous hab-itats 25–30 Ma (Kershaw et al., 1994; Martin, 2006). We furthernote that the Peltops lineage showed no evidence of concurrentdiversification (Fig. 3), which is consistent with the expectationthat lineages that primarily occur in open habitats would be morediverse than lineages restricted to mesic habitats (Byrne et al.,2011). However, it is important to note that we cannot rule outthe possibility that there have been extinctions of Peltops species,or any other mesic-restricted cracticine lineages in either Australiaor New Guinea. These patterns and timings of diversification with-in the Australo-Papuan cracticines parallel the timing of major


radiations of Australian sclerophyllous plant lineages (Crisp et al.,2004) and other similarly distributed Australo-Papuan birds (Toonet al., 2012) suggesting that the diversification of these diversegroups has been caused by similar factors.

Timings of divergence within Cracticus were consistent with theprediction of our second hypothesis that species that inhabit mon-soon savanna and arid, semi-arid and temperate open-woodlands(i.e. C. tibicen, C. nigrogularis, white-throated species group: C.argenteus, C. mentalis, C. torquatus) should have evolved after exten-sive stands of these habitats themselves appeared 6–8 Ma (Cerlinget al., 1997, 2011; Beerling and Osborne, 2006). Of particular impor-tance is the estimated timing of the divergence of the (1) C.tibicen + C. quoyi lineage and the hooded + white-throated lineagebetween 4.2–8.3 Ma, and (2) open grassland inhabiting C. tibicenand the closed mesic forest inhabiting C. quoyi between 3.0–5.8 Ma (Fig. 3). These observations parallel those of other recentstudies of widespread vertebrate and plant groups that revealeddiversifications of arid- and open grassland-adapted lineages dur-ing the late Miocene and early to mid Pliocene (e.g. Birds: Toonet al., 2012; Reptiles: Chapple et al., 2004; Kuch et al., 2005; Shooet al., 2008; Fujita et al., 2010; Marsupials: Blacket et al., 2000,2001; Meredith et al., 2008; Plants: Crisp and Cook, 2007).

Specific hypothesis-based tests of the impact of Plio-Pleistocenechanges in climate on the evolutionary history of C. quoyi, C. nigrog-ularis and C. tibicen have been addressed previously (Toon et al.,2007; Kearns et al., 2010, 2011). Key results include (1) genetic sig-natures of east–west divergence across regions that were puta-tively severely arid during the Pleistocene in species of bothtemperate, semi-arid and arid open woodlands (C. tibicen) and me-sic closed forests (C. quoyi) (Toon et al., 2007; Kearns et al., 2011),and (2) genetic signatures of recent range expansions and/or con-tractions in widespread species that inhabit temperate, semi-aridand arid open woodlands (C. tibicen, C. nigrogularis) (Toon et al.,2007; Kearns et al., 2010). Recent Plio-Pleistocene divergencesestimated between the hooded and white-throated species-groups(0.9–4.5 Ma), and between C. nigrogularis and C. cassicus (0.4–2.3 Ma) in this study (Fig. 3) add to the growing claims thatchanges in climate during the Plio-Pleistocene acted as a signifi-cant driver of speciation and diversification within Cracticus, aswell as for other widespread species across Australia (for reviewssee Byrne et al., 2008; Bowman et al., 2010).

4.2.2. Changes in sea-level: interchange between New Guinea andAustralia

The absence of detailed reconstructions of the timing of landconnections between Australia and New Guinea before 140 kya(Langford et al., 1995; Chappell et al., 1996; Veevers, 2000; Chivaset al., 2001; Hall, 2002; Sandiford, 2007; Heine et al., 2010) limitsour ability to explore the impact of early changes in sea-level onthe evolutionary history of the Australo-Papuan cracticines in ahypothesis testing framework. Shorelines are thought to have beenlargely similar to present-day shorelines during the Miocene andearly Pliocene (Veevers, 2000; Heine et al., 2010). The earliest Pli-ocene land connection between Australia and southern New Gui-nea is thought to have been present around 3.3 Ma — based onthe current depth of the Arafura shelf and estimates of globalsea-level curves (Chappell et al., 1996; Chivas et al., 2001; Naishet al., 2009). However, these global sea-level curve models do notaccount for ongoing north-westward subsidence of the Australianplate and so cannot provide a precise estimate of the timing of landconnections before 140 kya (Langford et al., 1995; Chappell et al.,1996; Veevers, 2000; Chivas et al., 2001; Sandiford, 2007; Heineet al., 2010). We therefore cannot evaluate whether the lack ofdivergences between Australian and New Guinean cracticine lin-eages between c. 5.8–17 Ma (Fig. 3) is attributable to the absenceof land connections that limited dispersal between the two land-

masses or to other factors such as extinction or the presence oftracts of unsuitable habitat that acted as barriers to dispersal de-spite the presence of land connections. Similar factors cannot beruled out in the case of the early divergence between New GuineanPeltops and mostly Australian-centred Strepera plus Cracticus line-age (17–28 Ma). That case could be interpreted to support thehypothesis that rainforest-inhabiting lineages were able to persistin isolation on the proto-New Guinean islands prior to the forma-tion of the current New Guinean landmass 2–5 Ma (Joseph et al.,2001; Krajewski et al., 2004; Westerman et al., 2006; Roelantset al., 2007; Malekian et al., 2010; Macqueen et al., 2010; JØnssonet al., 2011; Toon et al., 2012).

Over more recent timescales, timings of divergence betweenAustralian and New Guinean lineages within Cracticus accord withthe hypothesis that the savanna and grassland dominated landconnections between Australia and New Guinea during the Plio-Pleistocene facilitated the dispersal of open-habitat inhabitingspecies whereas these dry, open habitats represented a barrier todispersal for mesic-inhabiting species (sensu Ford, 1982) — i.e.divergence estimates for savanna-inhabiting C. mentalis (<0.14–0.38 Ma; Fig. 3) was substantially more recent than thoseestimated for the mesic-inhabiting C. quoyi (0.4–3.0 Ma; Fig. 3).Critically, however, we could not sample C. quoyi from southernNew Guinea (see Kearns et al., 2011). Thus, we cannot reject a sce-nario where mangroves and other small pockets of mesic-habitat,which were likely present on the exposed Arafura Shelf (Woodroffeet al., 1985; Van der Kaars, 1991; Woodroffe and Grindrod, 1991),facilitated recent dispersal between southern New Guinean andAustralian populations of C. quoyi. We were also unable to sampleC. tibicen specimens from southern New Guinea (see Amadon,1951; Black, 1986), however, given the open-habitat preferencesof this species it is likely that this population represents a recentlyisolated population that dispersed from Australia to New Guineaacross the open-habitat dominated land connections during thePlio-Pleistocene (Black, 1986). Finally, we note that the timing ofdivergence between Australian and New Guinean lineages of C.quoyi (0.4–3.0 Ma), and New Guinean C. cassicus and Australian C.nigrogularis (0.4–2.3 Ma) partially overlap (Fig. 3). This is intrigu-ing. In the absence of robust reconstructions of the inundation his-tory of the Arafura shelf for this time period (Veevers, 2000),however, we are unable to determine whether this temporal over-lap reflects a concerted response of these two partially co-occur-ring lineages to environmental changes in this region.

5. Conclusion

In this study we presented the first complete, well-supportedspecies-level phylogeny for the Australo-Papuan butcherbirdsand allies. Our study offers a good example of the advantages ofusing a multilocus coalescent approach to estimate evolutionaryrelationships and times of divergence when there is gene tree para-phyly and widespread sharing of alleles. By using this method we(1) provided a rigorous phylogenetically based assessment of therecent taxonomic decision to place the morphologically divergentAustralian Magpie C. tibicen in an expanded Cracticus (Christidisand Boles, 2008), (2) uncovered unexpected, complex patterns ofgenetic diversity in Peltops and the white-throated butcherbirdspecies-group that did not match current morphology-based spe-cies-boundaries, and (3) added to the growing number of studiesthat show complex spatial and temporal signatures of dispersal,population divergence and speciation within and between Austra-lia and New Guinea (e.g. Norman et al., 2002; Wüster et al., 2005;Murphy et al., 2007; Lee and Edwards, 2008; Williams et al., 2008;Zwiers et al., 2008; Toon et al., 2010, 2012; Macqueen et al., 2010;Pepper et al., 2011). These discordant genetic patterns could result


if species with different ecologies had different spatial and tempo-ral responses to environmental changes. However, more multilo-cus coalescent studies with dense taxon-sampling are required torule out alternative causes of discordance such as species-specific‘idiosyncratic’ responses or stochasticity in the lineage sortingprocess.

Acknowledgments

This research would not have been possible without the use ofspecimens from museum collections, accordingly we thank the fol-lowing collectors, collection managers and curators for the use ofspecimens in their care— Richard Schodde, Robert Palmer, AlexDrew, Lynn Pedler and Ian Mason (Australian National Wildlife Col-lection), Claire Stevenson and Ron Johnstone (Western AustralianMuseum), Rob Fleischer and Jack Dumbacher (SmithsonianInstitute), Vanessa Thompson, Joanna Sumner and Les Christidis(Museum of Victoria), Paul Sweet and Peg Hart (American Museumof Natural History), and Steve Donnellan (Australian Biological Tis-sue Collection/South Australian Museum). Thanks to Corinna Langefor providing laboratory space for DNA extractions and sequencingof toe-pad specimens, and the University of Queensland High Per-formance Computing Unit for the use of their facilities for computa-tionally intensive Bayesian analyses. Alicia Toon, Jane Hughes, AnneGoldizen, Cynthia Riginos and Terry Chesser provided advice andencouragement during various stages of this project. Researchwas funded by the Frank M. Chapman Memorial Fund of the Amer-ican Museum of Natural History, the Stuart Leslie Bird ResearchAward of Birds Australia, and The University of Queensland.Andrew Hugall, Robb Brumfield, Darren Irwin and an anonymousreviewer provided helpful comments on the manuscript.

Appendix A. Supplementary material

Supplementary data associated with this article can be found, inthe online version, at http://dx.doi.org/10.1016/j.ympev.2012.11.020.

References

Amadon, D., 1951. Taxonomic notes on the Australian butcher-birds (familyCracticidae). American Museum Novitates 1504, 1–33.

Barker, F.K., Cibois, A., Schikler, P., Feinstein, J., Cracraft, J., 2004. Phylogeny anddiversification of the largest avian radiation. Proceedings of the NationalAcademy of Sciences 101, 11040–11045.

Beerling, D.J., Osborne, C.P., 2006. The origin of the savanna biome. Global ChangeBiology 12, 2023–2031.

Beresford, P., Barker, F.K., Ryan, P.G., Crowe, T.M., 2005. African endemics span thetree of songbirds (Passeri): molecular systematics of several evolutionary‘enigmas’. Proceedings of the Royal Society B: Biological Sciences 272, 849–858.

Black, A.B., 1986. The taxonomic affinity of the New Guinean Magpie Gymnorhinatibicen papuana. Emu 86, 65–70.

Blacket, M.J., Adams, M., Krajewski, C., Westerman, M., 2000. Genetic variationwithin the dasyurid marsupial genus Planigale. Australian Journal of Zoology 48,443–459.

Blacket, M.J., Adams, M., Cooper, S.J.B., Krajewski, C., Westerman, M., 2001.Systematics and evolution of the dasyurid marsupial genus Sminthopsis: II.The Macroura species group. Journal of Mammalian Evolution 8, 149–170.

Bowler, J.M., 1982. Aridity in the late Tertiary and Quaternary of Australia. In:Barker, W.R., Greenslade, P.J.M. (Eds.), Evolution of the Flora and Fauna of AridAustralia. Peacock Publications, Adelaide, SA, pp. 35–45.

Bowman, D.M.J.S., Brown, G.K., Braby, M.F., Brown, J.R., Cook, L.G., Crisp, M.D., Ford,F., Haberle, S., Hughes, J., Isagi, Y., Joseph, L., McBride, J., Nelson, G., Ladiges, P.Y.,2010. Biogeography of the Australian monsoon tropics. Journal of Biogeography37, 201–216.

Byrne, M., Yeates, D.K., Joseph, L., Kearney, M., Bowler, J., Williams, M., Cooper, S.,Donnellan, S.C., Keogh, J.S., Leys, R., Melville, J., Murphy, D.J., Porch, N., Wyrwoll,K.H., 2008. Birth of a biome: insights into the assembly and maintenance of theAustralian arid zone biota. Molecular Ecology 17, 4398–4417.

Byrne, M., Steane, D.A., Joseph, L., Yeates, D.K., Jordan, G.J., Crayn, D., Aplin, K.,Cantrill, D.J., Cook, L.G., Crisp, M.D., Keogh, J.S., Melville, J., Moritz, C., Porch, N.,Sniderman, J.M.K., Sunnucks, P., Weston, P.H., 2011. Decline of a biome:

evolution, contraction, fragmentation, extinction and invasion of the Australianmesic zone biota. Journal of Biogeography 38, 1635–1656.

Carstens, B.C., Knowles, L.L., 2007. Estimating species phylogeny from gene treeprobabilities despite incomplete lineage sorting: an example from Melanoplusgrasshoppers. Systematic Biology 56, 400–411.

Cerling, T.E., Harris, J.M., MacFadden, B.J., Leakey, M.G., Quadek, J., Eisenmann, V.,Ehleringer, J.R., 1997. Global vegetation change through the Miocene/Plioceneboundary. Nature 389, 153–158.

Cerling, T.E., Wynn, J.G., Andanje, S.A., Bird, M.I., Korir, D.K., Levin, N.E., Mace, W.,Macharia, A.N., Quade, J., Remien, C.H., 2011. Woody cover and homininenvironments in the past 6 million years. Nature 476, 51–56.

Chappell, J., Omura, A., Esat, T., McCulloch, M., Pandolfi, J., Ota, Y., Pillans, B., 1996.Reconciliation of late Quaternary sea levels derived from coral terraces at HuonPeninsula with deep sea oxygen isotope records. Earth and Planetary SciencesLetters 141, 227–236.

Chapple, D.G., Keogh, J.S., Hutchinson, M.N., 2004. Molecular phylogeography andsystematics of the arid-zone members of the Egernia whitii (Lacertilia:Scincidae) species group. Molecular Phylogenetics and Evolution 33,549–561.

Chivas, A.R., Garcia, A., Van Der Kaars, S., Couapel, M.J.J., Holt, S., Reeves, J.M.,Wheeler, D.J., Switzer, A.D., Murray-Wallace, C.V., Banerjee, D., Price, D.M.,Wang, S.X., Pearson, G., Edgar, T., Beaufort, L., De Deckker, P., Lawson, E., Cecil,C.B., 2001. Sea-level and environmental changes since the last interglacial in theGulf of Carpentaria, Australia: an overview. Quaternary International 83, 19–46.

Christidis, L., Boles, W., 2008. Systematics and Taxonomy of Australian birdsCollingwood, Victoria, Australia. CSIRO Publishing.

Clement, M., Posada, D., Crandall, K.A., 2000. TCS: a computer program to estimategene genealogies. Molecular Ecology 9, 1657–1659.

Crisp, M., Cook, L., Steane, D., 2004. Radiation of the Australian flora: what cancomparisons of molecular phylogenies across multiple taxa tell us about theevolution of diversity in present-day communities? Philosophical Transactionsof the Royal Society B: Biological Sciences 359, 1551–1571.

Crisp, M.D., Cook, L.G., 2007. A congruent molecular signature of vicarianceacross multiple plant lineages. Molecular Phylogenetics and Evolution 43,1106–1117.

Crisp, M.D., Trewick, S.A., Cook, L.G., 2011. Hypothesis testing in biogeography.Trends in Ecology and Evolution 26, 66–72.

Deiner, K., Lemmon, A.R., Mack, A.L., Fleischer, R.C., Dumbacher, J.P., 2011. Apasserine Bird’s evolution corroborates the geologic history of the Island of NewGuinea. PLoS ONE 6, e19479, doi:19410.11371/journal.pone.0019479.

Dolman, G., Moritz, C., 2006. A multilocus perspective on refugial isolation anddivergence in rainforest skinks (Carlia). Evolution 60, 573–582.

Drummond, A.J., Rambaut, A., 2007. BEAST: bayesian evolutionary analysis bysampling trees. BMC Evolutionary Biology 7, 214.

Edwards, S.V., Beerli, P., 2000. Perspective: gene divergence, population divergence,and the variance in coalescence time in phylogeographic studies. Evolution 54,1839–1854.

Edwards, S.V., Liu, L., Pearl, D.K., 2007. High-resolution species trees withoutconcatentation. Proceedings of the National Academy of Sciences 104, 5936–5941.

Ericson, P.G.P., Christidis, L., Cooper, A., Irestedt, M., Jackson, J., Johansson, U.S.,Norman, J.A., 2002. A Gondwanan origin of passerine birds supported by DNAsequences of the endemic New Zealand wrens. Proceedings of the Royal SocietyB: Biological Sciences 269, 235–241.

Fjeldså, J., Bowie, R.C.K., Kiure, J., 2006. The forest batis, Batis mixta, is two species:description of a new, narrowly distributed Batis species in the Eastern Arcbiodiversity hotspot. Journal of Ornithology 147, 578–590.

Ford, J., 1979. A new subspecies of Grey Butcherbird from the Kimberley, WesternAustralia. Emu 79, 191–194.

Ford, J., 1982. Origin, evolution and speciation of birds specialized to mangroves inAustralia. Emu 82, 12–23.

Fuchs, J., Fjeldså, J., Pasquet, E., 2006. An ancient African radiation of corvoid birds(Aves: Passeriformes) detected by mitochondrial and nuclear sequence data.Zoologica Scripta 35, 375–385.

Fuchs, J., Bowie, R.C.K., Fjeldså, J., Pasquet, E., 2004. Phylogenetic relationships of theAfrican bush-shrikes and helmet-shrikes (Passeriformes: Malaconotidae).Molecular Phylogenetics and Evolution 33, 428–439.

Fuchs, J., Irestedt, M., Fjeldså, J., Couloux, A., Pasquet, E., Bowie, R.C.K., 2012.Molecular phylogeny of African bush-shrikes and allies: Tracing thebiogeographic history of an explosive radiation of corvoid birds. MolecularPhylogenetics and Evolution 64, 93–105.

Fujita, M.K., McGuire, J.A., Donnellan, S.C., Moritz, C., 2010. Diversificationand persistence at the arid-monsoonal interface. Australia-WideBiogeography of the Bynoe’s Gecko (Heteronotia binoei; Gekkonidae).Evolution 64, 2293–2314.

Hall, R., 2002. Cenozoic geological and plate tectonic evolution of SE Asia and theSW Pacific: computer-based reconstructions, model and animations. Journal ofAsian Earth Sciences 20, 353–431.

Heine, C., Müller, R.D., Steinberger, B., DiCaprio, L., 2010. Integrating deep Earthdynamics in paleogeographic reconstructions of Australia. Tectonophysics 483,135–150.

Heinsohn, T., Hope, G., 2006. The Torresian connections: zoogeography of NewGuinea. In: Merrick, J.R., Archer, M., Hickey, G.M., Lee, M.S.Y. (Eds.), Evolutionand Biogeography of Australian Vertebrates. Australian Scientific Publishing,Oatlands, NSW, pp. 71–93.




Heled, J., Drummond, A.J., 2010. Bayesian inference of species trees from multilocusdata. Molecular Biology and Evolution 27, 570–580.

Higgins, P.J., Peter, J.M., Cowling, S.J., 2006. Handbook of Australian, New Zealandand Antarctic Birds. Boatbill to Starlings, vol. 7. Oxford University Press,Melbourne.

Hope, G., Kershaw, A.P., Kaars, S.v.d., Xiangjun, S., Liew, P.-M., Heusser, L.E.,Takahara, H., McGlone, M., Miyoshi, N., Moss, P.T., 2004. History of vegetationand habitat change in the Austral-Asian region. Quaternary International 118–119, 103–126.

Huelsenbeck, J.P., Ronquist, F., 2001. MRBAYES: bayesian inference of phylogenetictrees. Bioinformatics 17, 754–755.

Jønsson, K.A., Fabre, P.-H., Ricklefs, R.E., Fjeldså, J., 2011. Major global radiation ofcorvoid birds originated in the proto-Papuan archipelago. Proceedings of theNational Academy of Sciences 108, 2328–2333.

Jønsson, K.A., Bowie, R.C.K., Nylander, J.A.A., Christidis, L., Norman, J.A., Fjeldså, J.,2010. Biogeographical history of cuckoo-shrikes (Aves: Passeriformes):transoceanic colonization of Africa from Australo-Papua. Journal ofBiogeography 37, 1767–1781.

Joseph, L., Slikas, B., Alpers, D., Schodde, R., 2001. Molecular systematics andphylogeography of New Guinean logrunners (Orthonychidae). Emu 101, 273–280.

Joseph, L., Toon, A., Schirtzinger, E.E., Wright, T.F., 2011. Molecular systematics oftwo enigmatic genera Psittacella and Pezoporus illuminate the ecologicalradiation of Australo-Papuan parrots (Aves: Psittaciformes). MolecularPhylogenetics and Evolution 59, 675–684.

Kass, R.E., Raftery, A.E., 1995. Bayes factors. Journal of the American StatisticalAssociation 90, 773–795.

Kearns, A.M., Joseph, L., Cook, L.G., 2010. The impact of Pleistocene changes ofclimate and landscape on Australian birds: a test using the Pied Butcherbird(Cracticus nigrogularis). Emu 110, 285–295.

Kearns, A.M., Joseph, L., Omland, K.E., Cook, L.G., 2011. Testing the effect of transientPlio-Pleistocene barriers in monsoonal Australo-Papua: did mangrove habitatsmaintain genetic connectivity in the Black Butcherbird? Molecular Ecology 20,5042–5059.

Kershaw, A.P., Martin, H.A., Mcewen Mason, J.R.C., 1994. The Neogene: a period oftransition. In: Hill, R.S. (Eds.), History of the Australian Vegetation: Cretaceousto Recent Cambridge University Press, Melbourne, pp. 299–327.

Knowles, L.L., 2009. Statistical Phylogeography. Annual Review of Ecology,Evolution, and Systematics 40, 593–612.

Krajewski, C., Moyer, G.R., Sipiorski, J.T., Fain, M.G., Westerman, M., 2004. Molecularsystematics of the enigmatic ‘phascolosoricine’ marsupials of New Guinea.Australian Journal of Zoology 52, 389–415.

Kuch, U., Keogh, J.S., Weigel, J., Smith, L.A., Mebs, D., 2005. Phylogeography ofAustralia’s king brown snake (Pseudechis australis) reveals Pliocene divergenceand Pleistocene dispersal of a top predator. Naturwissenschaften 92, 121–127.

Langford, R., Wilford, G., Truswell, E.M., Isern, A.R. 1995. Paleogeographic atlas ofAustralia. Volume 10 — Cainozoic, Australian Geological Survey Organization,Canberra.

Lee, J.Y., Edwards, S.V., 2008. Divergence across Australia’s Carpentarian barrier:statistical phylogeography of the red-backed fairy wren (Malurusmelanocephalus). Evolution 62, 3117–3134.

Macqueen, P., Seddon, J.M., Austin, J.J., Hamilton, S., Goldizen, A.W., 2010.Phylogenetics of the pademelons (Macropodidae: Thylogale) and historicalbiogeography of the Australo-Papuan region. Molecular Phylogenetics andEvolution 57, 1134–1148.

Maddison, W.P., Knowles, L.L., 2006. Inferring phylogeny despite incomplete lineagesorting. Systematic Biology 55, 21–30.

Malekian, M., Cooper, S.J.B., Norman, J.A., Christidis, L., Carthew, S.M., 2010.Molecular systematics and evolutionary origins of the genus Petaurus(Marsupialia: Petauridae) in Australia and New Guinea. MolecularPhylogenetics and Evolution 54, 122–135.

Manegold, A., 2008. Composition and phylogenetic affinities of vangas (Vangidae,Oscines, Passeriformes) based on morphological characters. Journal ofZoological Systematics and Evolutionary Research 46, 267–277.

Martin, D.P., Lemey, P., Posada, D., 2011. Analysing recombination in nucleotidesequences. Molecular Ecology Resources 11, 943–955.

Martin, H., 2006. Cenozoic climatic change and the development of the aridvegetation in Australia. Journal of Arid Environments 66, 533–563.

McCormack, J.E., Heled, J., Delaney, K.S., Peterson, A.T., Knowles, L.L., 2010.Calibrating divergence times on species trees versus gene trees: implicationsfor speciation history of aphelocoma jays. Evolution 65, 184–202.

Meredith, R.W., Westerman, M., Springer, M.S., 2008. A phylogeny and timescale forthe living genera of kangaroos and kin (Macropodiformes: Marsupialia) basedon nuclear DNA sequences. Australian Journal of Zoology 56, 395–410.

Milne, I., Wright, F., Rowe, G., Marshall, D., Husmeier, D., McGuire, G., 2004. TOPALi:software for automatic identification of recombinant sequences within DNAmultiple alignments. Bioinformatics 20, 1806–1807.

Moyle, R., Cracraft, J., Lakim, M., Nais, J., Sheldon, F., 2006. Reconsideration of thephylogenetic relationships of the enigmatic Bornean Bristlehead (Pityriasisgymnocephala). Molecular Phylogenetics and Evolution 39, 893–898.

Murphy, S.A., Double, M.C., Legge, S.M., 2007. The phylogeography of palmcockatoos, Probosciger aterrimus, in the dynamic Australo-Papuan region.Journal of Biogeography 34, 1534–1545.

Naish, T., Powell, R., Levy, R., Wilson, G., Scherer, R., Talarico, F., Krissek, L., Niessen,F., Pompilio, M., Wilson, T., Carter, L., DeConto, R., Huybers, P., McKay, R.,Pollard, D., Ross, J., Winter, D., Barrett, P., Browne, G., Cody, R., Cowan, E.,

Crampton, J., Dunbar, G., Dunbar, N., Florindo, F., Gebhardt, C., Graham, I.,Hannah, M., Hansaraj, D., Harwood, D., Helling, D., Henrys, S., Hinnov, L., Kuhn,G., Kyle, P., Läufer, A., Maffioli, P., Magens, D., Mandernack, K., McIntosh, W.,Millan, C., Morin, R., Ohneiser, C., Paulsen, T., Persico, D., Raine, I., Reed, J.,Riesselman, C., Sagnotti, L., Schmitt, D., Sjunneskog, C., Strong, P., Taviani, M.,Vogel, S., Wilch, T., Williams, T., 2009. Obliquity-paced Pliocene West Antarcticice sheet oscillations. Nature 458, 322–328.

Nicholls, J.A., Double, M.C., Rowell, D.M., Magrath, R.D., 2000. The evolution ofcooperative and pair breeding in thornbills Acanthiza (Pardalotidae). Journal ofAvian Biology 31, 165–176.

Norman, J.A., Christidis, L., Joseph, L., Slikas, B., Alpers, D., 2002. Unravelling abiogeographical knot: origin of the ‘leapfrog’ distribution pattern of Australo-Papuan sooty owls (Strigiformes) and logrunners (Passeriformes). Proceedingsof the Royal Society B: Biological Sciences 269, 2127–2133.

Norman, J.A., Ericson, P.G.P., Jønsson, K.A., Fjeldså, J., Christidis, L., 2009. A multi-gene phylogeny reveals novel relationships for aberrant genera of Australo-Papuan core Corvoidea and polyphyly of the Pachycephalidae andPsophodidae (Aves: Passeriformes). Molecular Phylogenetics and Evolution52, 488–497.

Nylander, J.A.A., 2004. MrModeltest v2, Program Distributed by the Author,Evolutionary Biology Centre. Uppsala University, Sweden.

Nylander, J.A.A., Ronquist, F., Huelsenbeck, J., Nieves-Aldrey, J., 2004. Bayesianphylogenetic analysis of combined data. Systematic Biology 53, 47–67.

Parchman, T.L., Benkman, C.W., Britch, S.C., 2006. Patterns of genetic variation in theadaptive radiation of New World crossbills (Aves: Loxia). Molecular Ecology 15,1873–1887.

Pepper, M., Fujita, M.K., Moritz, C., Keogh, J.S., 2011. Palaeoclimate change drovediversification among isolated mountain refugia in the Australian arid zone.Molecular Ecology 20, 1529–1545.

Pigram, C.J., Davies, H.L., 1987. Terranes and the accretion history of the NewGuinea Orogen. BMR Journal of Australian Geology Geophysics 10, 193–211.

Rambaut, A., Drummond, A.J. (2007). Tracer v1.4. <http://beast.bio.ed.ac.uk/Tracer>(accessed 20.10.11).

Reddy, S., Driskell, A., Rabosky, D.L., Hackett, S.J., Schulenberg, T.S., 2012.Diversification and the adaptive radiation of the vangas of Madagascar.Proceedings of the Royal Society B: Biological Sciences. http://dx.doi.org/10.1098/rspb.2011.2380.

Roelants, K., Wilkinson, M., Loader, S.P., Biju, S.D., Guillaume, K., Moriau, L., Bossuyt,F., 2007. Global patterns of diversification in the history of modern amphibians.Proceedings of the National Academy of Sciences 104, 887–892.

Russell, E., Rowley, I., 2009. Family Cracticidae (Butcherbirds). In: Del Hoyo, J.,Elliott, A., Christie, D. (Eds.), Handbook of the Birds of the World, Bush-shrikesto Old World Sparrows, vol. 14. Barcelona, Lynx Edicions, pp. 308–342.

Sandiford, M., 2007. The tilting continent: a new constraint on the dynamictopographic field from Australia. Earth and Planetary Science Letters 261, 152–163.

Sato, A., O’Huigin, C., Figueroa, F., Grant, P.R., Grant, B.R., Tichy, H., Klein, J., 1999.Phylogeny of Darwin’s finches as revealed by mtDNA sequences. Proceedings ofthe National Academy of Sciences 96, 5101–5106.

Schodde, R., 1989. Origins, radiations and sifting in the Australasian biota: changingconcepts from new data and old. Australian Systematic Botany SocietyNewsletter 60, 2–11.

Schodde, R., 2006. Australia’s bird fauna today — origins and development. In:Merrick, J.R., Archer, M., Hickey, G.M., Lee, M.S.Y. (Eds.), Evolution andBiogeography of Australasian Vertebrates. AusciPub, Sydney, pp. 413–458.

Schodde, R., Calaby, J.H., 1972. The biogeography of the Australo-Papuan bird andmammal faunas in relation to Torres Strait. In: Walker, D. (Ed.), Bridge andBarrier: The Natural and Cultural History of Torres Strait. Australian NationalUniversity, Canberra, pp. 257–300.

Schodde, R., Mason, I.J., 1999. The Directory of Australian Birds: Passerines. CSIROPublishing, Melbourne.

Shoo, L.P., Rose, R., Doughty, P., Austin, J.J., Melville, J., 2008. Diversification patternsof pebble-mimic dragons are consistent with historical disruption of importanthabitat corridors in arid Australia. Molecular Phylogenetics and Evolution 48,528–542.

Stamatakis, A., 2006. RAxML-VI-HPC: maximum likelihood-based phylogeneticanalyses with thousands of taxa and mixed models. Bioinformatics 22, pp.2688–2690.

Stephens, M., Donnelly, P., 2003. A comparison of bayesian methods for haplotypereconstruction from population genotype data. The American Journal of HumanGenetics 73, 1162–1169.

Storr, G.M., 1952. Remarks on the Streperidae. South Australian Ornithologist 20,78–80.

Toon, A., Hughes, J.M., Joseph, L., 2010. Multilocus analysis of honeyeaters (Aves:Meliphagidae) highlights spatio-temporal heterogeneity in the influence ofbiogeographic barriers in the Australian monsoonal zone. Molecular Ecology 19,2980–2994.

Toon, A., Mather, P.B., Baker, A.M., Durrant, K.L., Hughes, J.M., 2007. Pleistocenerefugia in an arid landscape: analysis of a widely distributed Australianpasserine. Molecular Ecology 16, 2525–2541.

Toon, A., Austin, J., Dolman, G., Pedler, L., Joseph, L., 2012. Evolution of arid zonebirds in Australia: leapfrog distribution patterns and mesic-arid connections inquail-thrush. Molecular Phylogenetics and Evolution 62, 286–295.

Van der Kaars, W.A., 1991. Palynology of eastern Indonesian marine piston-cores: aLate Quaternary vegetational and climatic record for Australasia.Palaeogeography, Palaeoclimatology, Palaeoecology 85, 239–252.

http://beast.bio.ed.ac.uk/Tracer

http://dx.doi.org/10.1098/rspb.2011.2380

http://dx.doi.org/10.1098/rspb.2011.2380


Veevers, J., 2000. Billion-Year Earth History of Australia and Neighbours inGondwanaland. GEMOC Press, Sydney.

Weir, J.T., Schluter, D., 2008. Calibrating the avian molecular clock. MolecularEcology 17, 2321–2328.

Westerman, M., Young, J., Donnellan, S., Woolley, P.A., Krajewski, C., 2006.Molecular relationships of new guinean three-striped dasyures, (Myoictis,Marsupialia: Dasyuridae). Journal of Mammalian Evolution 13, 211–222.

Williams, D.J., O’Shea, M., Daguerre, R.L., Pook, C.E., Wüster, W., Hayden, C.J., McVay,J.D., Paiva, O., Matainaho, T.L., Winkel, K.D., Austin, C.C., 2008. Origin of theeastern brownsnake, Pseudonaja textilis (Duméril, Bibron andDuméril)(Serpentes: Elapidae: Hydrophiinae) in New Guinea: evidence ofmultiple dispersals from Australia, and comments on the status of Pseudonajatextilis pughi Hoser 2003. Zootaxa 1703, 47–61.

Williams, M., Cook, E., van der Kaars, S., Barrows, T., Shulmeister, J., Kershaw, P.,2009. Glacial and deglacial climatic patterns in Australia and surroundingregions from 35000 to 10000 years ago reconstructed from terrestrial and near-shore proxy data. Quaternary Science Reviews 28, 2398–2419.

Woodroffe, C.D., Grindrod, J., 1991. Mangrove biogeography: the role of quaternaryenvironmental and sea-level change. Journal of Biogeography 18, 479–492.

Woodroffe, C.D., Thom, B.G., Chappell, J., 1985. Development of widespreadmangrove swamps in mid-Holocene times in northern Australia. Nature 317,711–713.

Wüster, W., Dumbrell, A.J., Hay, C., Pook, C.E., Williams, D.J., Fry, B.G., 2005. Snakesacross the Strait: trans-Torresian phylogeographic relationships in three generaof Australasian snakes (Serpentes: Elapidae: Acanthophis, Oxyuranus, andPseudechis). Molecular Phylogenetics and Evolution 34, 1–14.

Yamagishi, S., Honda, M., Eguchi, K., Thorstrom, R., 2001. Extreme endemic radiationof the Malagasy Vangas (Aves: Passeriformes). Journal of Molecular Evolution53, 39–46.

Zachos, J., 2001. Trends, rhythms, and aberrations in global climate 65 ma topresent. Science 292, 686–693.

Zwiers, P.B., Borgia, G., Fleischer, R.C., 2008. Plumage based classification of thebowerbird genus Sericulus evaluated using a multi-gene, multi-genomeanalysis. Molecular Phylogenetics and Evolution 46, 923–931.

A multilocus coalescent analysis of the speciational history of the Australo-Papuan butcherbirds and...

Documents

Transcript of A multilocus coalescent analysis of the speciational history of the Australo-Papuan butcherbirds and...