Zoologica Scripta

Out of the Bassian province: historical biogeography of the Australasian platycercine parrots (Aves, Psittaciformes)

MANUEL SCHWEIZER,MARCEL GU¨ NTERT &STEFAN T. HERTWIG

Submitted: 6 March 2012 Schweizer, M., Gu¨ntert, M. & Hertwig, S. T. (2012). Out of the Bassian province: histori- Accepted: 2 July 2012 cal biogeography of the Australasian platycercine parrots (Aves, Psittaciformes). —Zoologica doi:10.1111/j.1463-6409.2012.00561.x Scripta, 00, 000–000. Aridification from mid-Miocene onwards led to a fragmentation of mesic biomes in Aus- tralia and an expansion of arid habitats. This influenced the diversification of terrestrial organisms, and the general direction of their radiations is supposed to have been from mesic into drier habitats. We tested this hypothesis in the platycercine parrots that occur in different habitats in Australia and also colonized Pacific islands. We inferred their tem- poral and spatial diversification patterns using a Bayesian relaxed molecular clock approach based on three nuclear and two mitochondrial genes and model-based biogeographic reconstructions. The Bassian biota was found to be the centre of origin of platycercine parrots and diversification within two of their three clades coincided with the beginning of aridification of Australia. The associated habitat changes may have catalysed their radiation through adaptation to arid environments and vicariance because of the fragmentation of non-arid habitats. The small oceanic islands of Melanesia contributed as stepping stones for the colonization of New Zealand from Australia. Corresponding author: Manuel Schweizer, Naturhistorisches Museum der Burgergemeinde Bern, Bernastrasse 15, CH 3005 Bern, Switzerland. E-mail: [email protected] Stefan T. Hertwig and Marcel Gu¨ntert, Naturhistorisches Museum der Burgergemeinde Bern, Bernastrasse 15, CH 3005 Bern, Switzerland. E-mails: [email protected], marcel.guentert@ nmbe.ch High Taxon Name: Aves, Psittaciformes, Platycercinae No new taxa described.

Introduction much of the Australian continent (Jacobs et al. 1999; The avifauna of the Australasian region and especially of Martin 2006; Schodde 2006). The general direction of its oceanic islands has played an important role for the radiation for land birds and other taxonomic groups in development of theories on speciation and biogeography Australasia has been suggested to be from rainforests into as well as the evolution of continental biota (Cracraft drier and more open habitats (Schodde 2006; Byrne et al. 1986; Filardi & Moyle 2005; Mayr & Diamond 2001; 2008, 2011). Ancestors of recent arid taxa may have either McDowall 2008; Wallace 1867). The core of the Austral- diverged from their closest relatives before the onset of asian bird fauna has a Gondwana origin and has radiated aridification and adapted to arid environment in situ or in isolation during the Palaeogene under the influence of originated from mesic ancestors through multiple diversifi- climate and environmental change as well as tectonic activ- cation and colonization events of arid regions (reviewed in ities (Schodde 2006; Christidis & Norman 2010; Trewick Byrne et al. 2008). The fragmentation of mesic biomes & Gibb 2010). The aridification of the Australian conti- moreover led to localized endemism and phylogeographic nent beginning in the middle Miocene or perhaps even structure in taxa specialized on these habitats (cf. e.g. earlier seems to have had a major influence on the diversi- Schodde 2006; Byrne et al. 2011). fication of the Australian bird fauna (Schodde 2006; Byrne Parrots are one of the dominant elements of the Eyrean et al. 2011). Then, a major change of vegetation began in avifauna of the arid parts of Australia (Schodde 2006), and Australia with shrinkage of rainforests, fragmentation of especially, members of the cockatoos and of the broad- mesic biomes and an expansion of drier, more open sclero- tailed or platycercine parrots (Platycercinae, consisting of phyll forests. Today, arid and semi-arid habitats cover Pezoporini and Platycercini, Joseph et al. (2012)) are today

ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters 1 Biogeography of Australasian platycercine parrots d M. Schweizer et al. adapted to dry environments (Collar 1997; Rowley 1997). sampling was based on the study by Schweizer et al. (2011), The diversification of cockatoo genera occurred during but we added two fast-evolving mitochondrial genes (partly the early Miocene to Pliocene, and the contemporaneous used for outgroup taxa in Schweizer et al. 2012) to the three aridification may have promoted their radiation and the nuclear exons analysed in the latter study and included convergent evolution of specific morphological adaptations moreover three additional species within Platycercinae such as plumage colour, body size, wing shape and bill (Barnardius barnardi, Psephotus haematonotus and Pezoporus structure across different lineages of cockatoos (White wallicus). We used a relaxed molecular clock approach and et al. 2011). The beginning of the radiation of the platy- model-based ancestral area reconstructions to uncover his- cercine genera that comprise species adapted to arid habi- torical and biogeographic patterns. tats also seems to have coincided with the onset of the aridification of Australia (Schweizer et al. 2011). Today, Material and methods the Platycercinae occur in a variety of habitats in the Aus- Sampling and laboratory methods tralian continent with the exception of the Tumbunan and We obtained tissue or feather samples from 35 species of Irian rainforests and occupy also several islands in Melane- Old World parrots complemented with sequences from sia and the South Pacific including New Zealand (Collar GenBank (Table 1). We included all species of the ‘core 1997; Schodde 2006). Christidis et al. (1991) proposed two platycercines’ with the exception of the almost certainly successive radiations of Platycercinae, a first continent- extinct paradise parrot Psephotus pulcherrimus (Collar 1997) wide from mid-Miocene involving the divergence of Pezop- and four species of the well-defined monophyletic genus orus, Melopsittacus, Neopsephotus, Neophema and the ‘core Platycercus (Joseph et al. 2008). The different genera of the platycercines’ (Platycercus, Barnardius, Northiella, Purpurei- ‘core platycercines’ consist of the following number of cephalus, Psephotus and Lathamus) and the spread of ances- species and subspecies: Purpureicephalus, 1 monotypic spe- tors of Prosopeia, Cyanoramphus and Eunymphicus to Pacific cies; Barnardius, 2 species and 3 subspecies; Platycercus,8 islands. A second radiation concerned the diversification of species and 15 subspecies; Northiella, one species and four the ‘core platycercines’ and was supposed to have been subspecies; Psephotus, five species and six subspecies. More- centred in the eucalypt-dominated Bassian biota found over, we included samples of all remaining seven platycer- today in southern Australia with subsequent colonization cine genera and potentially affiliated Australasian taxa, and of arid regions and the monsoon woodlands in the north. Nestor notabilis was chosen as outgroup (cf. de Kloet & de Reconstructions of the direction of radiations are heavily Kloet 2005; Wright et al. 2008; Schweizer et al. 2010, based on phylogenetic hypothesis and are only as good as 2011). The taxonomy of Collar (1997) is followed here, the phylogenetic reconstruction which they are based upon although we include ‘Geopsittacus’inPezoporus (Joseph (Schodde 2006). The scenario formulated by Christidis et al. 2011) and follow the recommendations of Boon et al. et al. (1991) was based on allozyme data and did not rely (2001) for Cyanoramphus. For family-group taxa, we follow on an explicit temporal and spatial framework. In the Joseph et al. (2012). meantime, the results of not only several recent molecular Total genomic DNA was isolated using peqGOLD tis- phylogenetic, but also morphological studies have rear- sue DNA Mini Kit (Peqlab, Germany) or DNeasy Blood ranged the relationships of Platycercinae and other Aus- & Tissue Kit (Qiagen, Switzerland) following manufac- tralasian parrots with some controversial issues still turer’s instruction. Partial sequences of the three nuclear remaining. Importantly, Melopsittacus does not belong to genes c-mos, RAG-1 and Zenk (second exon) and the two Platycercini and is closely related to the lories, while Lath- mitochondrial genes ND2 (NADH2) and Cytb (cytochrome amus seems to be more closely related to Cyanoramphus, b) were amplified with polymerase chain reaction (PCR) Prosopeia and Eunymphicus than to the ‘core platycercines’ using published primer sequences (Table 2). PCR volumes (Wright et al. 2008; Schweizer et al. 2010, 2011; Joseph were 20 lL containing 10 lL PCR-Master-Mix S (c-mos), et al. 2011). PCR-Master-Mix Y (RAG-1, Zenk, ND2) or HotStart- In the present study, we aimed at reconstructing the radi- Master-Mix (Cytb) (Peqlab), 2–3 lL genomic DNA, 2 lL ation of Platycercinae-based on a spatial and temporal of each primer with a concentration of 10 lM and 3–4 lL framework. We tested the hypothesis on their radiation for- ddH2O. PCR was performed on a Techne TC-512 mulated by Christidis et al. (1991) and the assumption by thermo-cycler. Amplification of c-mos was performed with Byrne et al. (2011) that mesic biomes should be ancestral in the following parameters: initial denaturation of 94 C for Australian taxa containing both mesic and arid ⁄ monsoon 2 min followed by 33 cycles of denaturation at 90 C for zone representatives. We therefore constructed a molecular 30 s, annealing at 55 C for 30 s and extension at 72 C phylogeny of the platycercine parrots using three nuclear for 1 min, with a final extension at 72 C for 5 min. The and two mitochondrial markers. The taxon and character PCR profile published by Groth & Barrowclough (1999)

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Table 1 Species sampled, Museum and collection number, GenBank Accession numbers for the five genes analysed

Species Museum ⁄ Collection Collection no. c-mos RAG-1 Zenk ND2 Cytb

Apaporis roseicollis NMBE (except ND2) 1056204 GQ505086 GQ505194 GQ505141 EU327596 JQ066204 Barnardius zonarius NMBE 1056210 GQ505095 GQ505203 GQ505149 JQ066250 JQ066207 Barnardius barnardi NMBE 1059100 – JX442402 – JX442398 JX442433 Charmosyna pulchella NMBE 1056241 GQ505126 GQ505237 GQ505179 JX442396 JX442429 Cyanoramphus auriceps NMBE 1056221 GQ505104 GQ505213 GQ505158 JX442387 JX442418 Cyanoramphus novaezelandiae NMBE 1056220 GQ505103 GQ505212 GQ505157 JQ066252 JQ066210 Eclectus roratus NMBE (except ND2) 1056248 GQ505135 GQ505244 GQ505187 EU327619 JQ066219 Eos cyanogenia NMBE 1056237 GQ505122 GQ505233 GQ505175 JQ066254 JQ066215 Eunymphicus cornutus cornutus NMBE 1056223 GQ505106 GQ505215 GQ505159 JX442388 JX442421 Eunymphicus cornutus uvaeensis NMBE 1056224 GQ505107 GQ505216 GQ505160 JX442389 JX442422 Lathamus discolor NMBE 1056219 GQ505102 GQ505211 GQ505156 JX442385 JX442416 Loriculus galgulus UWBM (except ND2) 73841 ⁄ 2002-006 GQ505089 GQ505196 – EU327631 JQ066205 Lorius garrulus NMBE 1056240 GQ505125 GQ505236 GQ505178 JQ066256 JQ066216 Melopsittacus undulatus UWBM (except ND2) 60748 ⁄ 1998-068 – GQ505222 GQ505166 EU327633 JQ066214 Micropsitta finschii tristrami UWBM (except ND2) 66040 ⁄ 2000-022 GQ505128 GQ505240 GQ505182 EU327634 JQ066218 Neophema chrysostoma NMBE 1056228 GQ505111 GQ505220 GQ505164 JX442392 JX442425 Neophema pulchella NMBE 1056226 GQ505109 GQ505218 GQ505162 JX442391 JX442424 Neophema splendida NMBE 1056225 GQ505108 GQ505217 GQ505161 JQ066253 JQ066212 Neopsephotus bourkii UWBM (except ND2) 57542 ⁄ 1996-109 GQ505112 GQ505221 GQ505165 EU327639 JQ066213 Nestor notabilis NMBE (except ND2) 1056242 JF807958 GQ505238 GQ505180 EU327641 JQ066203 Northiella haematogaster NMBE 1056954 JF807959 JF807986 JF807972 JX442397 EU327641 Pezoporus wallicus ANWC 45982 HQ316825 HQ316839 HQ316854 HQ316878 HQ324422 Platycercus caledonicus NMBE (except ND2) 1056212 GQ505097 GQ505205 GQ505151 EU407679 JQ066208 Platycercus eximius NMBE (except ND2) 1056213 – GQ505206 GQ505152 EU407711 JX442412 Platycercus flaveolus NMBE (except ND2) 1056215 GQ505099 GQ505208 – EU407696 JX442434 Platycercus venustus NMBE 1056214 GQ505098 GQ505207 GQ505153 JX442382 JX442413 Polytelis alexandrae NMBE (except ND2) 1056209 GQ505093 GQ505201 GQ505147 EU327653 JQ066206 Prosopeia tabuensis NMBE (except ND2) 1056252 GQ505105 GQ505214 – EU327656 JQ066211 Psephotus chrysopterygius NMBE 1056953 JF807963 JF807991 JF807977 JX442400 JX442436 Psephotus dissimilis NMBE 1056218 GQ505101 GQ505210 GQ505155 JX442384 JX442415 Psephotus haematonotus NMBE 1059101 JX442404 JX442403 JX442379 JX442399 JX442435 Psephotus varius NMBE 1056217 GQ505100 GQ505209 GQ505154 JQ066251 JQ066209 Psittacella brehmii KU 12931 ⁄ 91954 JF807964 JF807992 JF807978 JQ066258 JQ066220 Psitteuteles goldiei NMBE (except Cytb) 1056239 GQ505124 GQ505235 GQ505177 JQ066255 AF346343 Purpureicephalus spurius NMBE 1056211 GQ505096 GQ505204 GQ505150 JX442381 JX442410 was used for RAG-1 with the initial denaturation step cleaning. Sequencing was carried out using Microsynth reduced to 2 min. For Zenk, the PCR profile of Chubb AG (Balgach, Switzerland). Cytb was sequenced using the (2004) was used with the annealing temperature set to primer L15132, while the other four genes were sequenced 53.5 C. The PCR Protocol of Tavares et al. (2006) with from both sides using the same primers as for amplifica- the annealing temperature set to 53 was applied for tion leading to complete overlapping fragments for RAG- ND2. Amplification of Cytb was performed with an initial 1 and c-mos and an overlapping fragment of about 600 bp denaturation of 94 C for 3 min followed by 35 cycles of for Zenk and of about 500 bp for ND2. Sequencing files denaturation at 95 C for 30 s, annealing at 54.5 C for were checked using Chromas (Technelysium Pty. Ltd.), 30 s and extension at 72 C for 1 min, with a final exten- and ambiguities were assigned standard IUB codes. The sion at 72 C for 7 min. PCR products were examined by alignment of the sequences was made manually after trans- gel electrophoresis to confirm the amplification of the lation of the sequences into amino acids with BIOEDIT target fragment. PCR products were either excised from 7.0.5.2 (Hall 1999). We checked individual sequences and gels and cleaned using the Wizard SV Gel and PCR the whole alignment further for apparent stop codons and Clean-UP System (Promega, Switzerland) or directly puri- for indels that were not a multiple of three bases. fied with the above-mentioned kit or with the peqGOLD MicroSpin Cycle-Pure Kit (Peqlab). To increase the quan- Phylogenetic analyses tity of DNA for problematic samples, the products of two Nuclear and mitochondrial markers were analysed com- independent PCR runs were put together before the bined and separately throughout. Bayesian inference was

ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters 3 Biogeography of Australasian platycercine parrots d M. Schweizer et al.

Table 2 Primers used for the amplification of the five genes 2008) with all free model parameters estimated by the analysed in this study software (substitution rates, gamma shape parameter, base frequencies) using the best parameter setting as obtained Gene Primer name Reference with MRBAYES. For the maximum parsimony analyses, we c-mos F944 (Cooper & Penny 1997) conducted heuristic searches in PAUP* (Swafford 2001) R1550or05 (Overton & Rhoads 2004) (1000 random taxon-addition replicates, TBR branch R1550hb99 (Hughes & Baker 1999) swapping) with gaps treated as a fifth character state. RAG-1 R8 (Groth & Barrowclough 1999) Nodal support was estimated with a maximum parsimony R11B (Groth & Barrowclough 1999) R17 (Groth & Barrowclough 1999) bootstrap analysis (1000 pseudo-replicates, heuristic R18 (Groth & Barrowclough 1999) search, 10 random taxon-addition replicates, TBR branch Zenk Z1F (Chubb 2004) swapping, number of max trees limited to 100). We con- Z9R (Chubb 2004) sidered clades as being supported when the clade credibil- ND2 MetL (Tavares et al. 2006) ity values of the Bayesian inference were ‡0.95 ASNH (Tavares et al. 2006) Cytb L15132 (Boon et al. 2000) (Huelsenbeck & Ronquist 2001) and when bootstrap val- H16065 (Boon et al. 2000) ues were ‡70 in the maximum-likelihood and maximum parsimony analyses (Hillis & Bull 1993). conducted in MRBAYES 3.2 (Huelsenbeck & Ronquist Molecular dating 2001; Ronquist & Huelsenbeck 2003) using a mixed- Divergence times were estimated using BEAST 1.6.1 model approach. We evaluated alternative biologically rel- (Drummond & Rambaut 2007). We applied a relaxed evant parameter settings corresponding to separate models molecular clock with uncorrelated lognormal distribution with varying base frequencies, rate matrix, shape parame- of branch lengths and a Yule tree prior with the best ters and proportion of invariable sites for the concatenated parameter setting found via the MRBAYES analyses and the data and the different genes and ⁄ or their codon positions. respective nucleotide substitution models as evaluated in Nucleotide substitution models were evaluated with MRMODELTEST. MrModeltest 2.3 (Nylander 2004) using the Akaike infor- As there are no representative fossil parrots which could mation criterion (Akaike 1974). We performed two inde- provide prior distributions for primary calibrations (cf. pendent runs of Metropolis-coupled Markov chain Monte Mayr 2009; Schweizer et al. 2011), the calibration adopted Carlo analyses for each parameter setting, each run con- was based on a molecular dating analysis of the parrots sisting of one cold chain and three heated chains with a which was calibrated with well-accepted avian fossils out- default temperature of 0.2. The chains were run for 10 side the parrots (Schweizer et al. 2011). According to the million generations with sampling every 100 generations. results of this study, we used a mean estimate of 58 Ma We verified that the average standard deviation of split (millions of years ago) with a normal distribution frequencies converged towards zero and calculated the (95% ± about 20 million years or SD = 10) for the initial length of ‘burn-in’ by monitoring the change in cumula- split within the crown group parrots separating Nestor tive split frequencies using AWTY (Nylander et al. 2008; (and Strigops) from the remaining taxa. This time interval Wilgenbusch et al., 2004). We then discarded the first also includes similar estimates of other studies for the ini- 25% of samples as burn-in (25 000 trees). Moreover, we tial split within crown group parrots based on fossil cali- compared likelihoods and posterior probabilities of all brations (Pratt et al. 2009; Pacheco et al. 2011; White splits and parameters to assess convergence among the two et al. 2011). Moreover, Platycercini were defined as being independent runs using AWTY and TRACER 1.5 (Rambaut & monophyletic and their initial split was used as a second Drummond 2007). We used the Bayes Factor (BF) to eval- calibration point with a mean estimate of 20 Ma and a uate the relevance of the different parameter settings (Kass normal distribution (95% ± about 9 million years or & Raftery 1995; Brown & Lemmon 2007). The harmonic SD = 4.5) again based on the results of Schweizer et al. mean calculated by MRBAYES was used as an estimation of (2011). Default prior distributions were chosen for all the marginal likelihood of the data (Kass & Raftery 1995). other parameters, and the MCMC was run for 25 million A more complex model (i.e. more parameters) was consid- generations with sampling every 1000 generations. We ered to be more supported compared to a simpler model used TRACER 1.5 (Rambaut & Drummond 2007) to con- if 2lnBF was >10 (Brown & Lemmon 2007). We employed firm appropriate burn-in and the adequate effective sample RAxML 7.0.4 (Stamatakis 2006) for the maximum-likeli- sizes of the posterior distribution. Two independent chains hood (ML) search. The software was run on the web ser- were run, and we compared likelihoods and posterior ver with 100 rapid bootstrap inferences (Stamatakis et al. probabilities of all parameters to assess convergence

4 ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters M. Schweizer et al. d Biogeography of Australasian platycercine parrots

among the runs using TRACER. The resulting maximum and all combinations of areas were allowed in the adja- clade credibility tree and the 95% highest posterior den- cency matrix. Baseline rates of dispersal and local extinc- sity (HPD) distributions of each estimated node were visu- tion were estimated by the software. alized using FIGTREE 1.2.1 (Rambaut 2008). Results Biogeographic reconstruction Phylogenetic analyses We used the likelihood approach of the software Lagrange The final alignment consisted of 5121 bp with 603 stem- to reconstruct the biogeographic history of the platycer- ming from c-mos, 1458 from RAG-1, 1143 from Zenk, 876 cine parrots (Snapshot version for web configuration tool from Cytb and 1041 from ND2. It contained one indel of at http://www-reelab.net/lagrange) (Ree et al. 2005; Ree & two and one indel of three amino acids for RAG-1 and Smith 2008). The reconstruction was based on the maxi- one indel of one amino acid for Zenk. Different models of mum clade credibility tree obtained in BEAST. We were nucleotide evolution were selected for the different parti- primarily interested in the biogeographic history of Platyc- tions of our data set (Table 3). ercinae; thus, all other taxa were pruned from the tree. Combined analyses: the parameter setting using differ- Lagrange treats dispersal and local extinctions as stochastic ent models of sequence evolution for the five genes and processes incorporating a continuous-time model for geo- three codon positions was chosen as the best-fitting model graphic range evolution through dispersal, extinction and after the calculation of the Bayes Factors. Based on this cladogenesis (DEC model) (Ree et al. 2005; Ree & Smith parameter setting, the analysis was rerun for 20 million 2008; Ree & Sanmartin 2009). According to their current generations with the temperature set to 0.1. Most basal distribution (Collar 1997), the zoogeographic delimitation nodes were not supported in the resulting 50% majority- of Merrick et al. (2006) and the classification of Schodde rule consensus tree (Fig. 1), and also the monophyly of (2006), the taxa were assigned to the following biogeo- Platycercinae was not robustly supported. Platycercini graphic provinces (avifaunulas): Melanesia (Fiji, Tonga, were divided into two well-supported clades in congruence New Caledonia), New Zealand as well as Bassian, Eyrean with Schweizer et al. (2010, 2011) and Joseph et al. (2011). and Torresian regions. Bassian taxa occur in sclerophyl- The relationship of Prosopeia was not robustly supported lous forests and woodlands of south, south-west and as in the study by Schweizer et al. (2010, 2011). However, south-east Australia as well as Tasmania, while Eyrean its position within its clade was in congruence with the taxa occupy the dry areas of inland and western Australia study by Joseph et al. (2011) where it was robustly sup- (mulga woodlands, spinifex dune deserts and dry stony ported. Within the ‘core platycercines’, Purpureicephalus ranges). Torresian species are confined to monsoonal spurius clustered together with Psephotus varius, P. dissimilis eucalypt and paperbark woodlands in northern Australia and P. chrysopterygius, but Psephotus haematonotus did not (Schodde 2006) (Fig. 3). Pezoporus wallicus occurs in Bas- cluster with the remaining species of its genus. However, sian biota, and Pezoporus occidentalis, its sister taxon (Joseph its position, as well as that of Northiella haematogaster, was et al. 2011), is an Eyrean species (Schodde 2006). There- not robustly supported. The topology of the best-scoring fore, both biogeographic provinces were assigned to Pezop- maximum-likelihood tree was similar to the 50% majority- orus. As distribution of parrots may have spanned over rule consensus tree of the Bayesian inference (Fig. 1). more than one biogeographic area in the past as in some However, Purpureicephalus spurius and Psephotus varius were species today, the maximum range size was not restricted revealed as sister taxa, although this clade was not

Table 3 Sequence evolution models for the five different genes and their different partitions analysed

Model

Number of bp All 1 pos 1 & 2 pos 2 pos 3 pos c-mos 603 GTR + G HKY HKY + G K80 + I HKY + G RAG-1 1458 GTR + I + G HKY + G GTR + I + G GTR + I HKY + G Zenk 1143 HKY + I HKY + I HKY + I HKY HKY + G Cytb 876 GTR + I + G SYM + G GTR + I + G GTR + I + G GTR + G ND2 1041 GTR + I + G GTR + I + G GTR + I + G HKY + I + G GTR + I + G Combined data set 5121 GTR + I + G Nuclear markers 3204 HKY + I + G Mitochondrial markers 1917 GTR + I + G

ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters 5 Biogeography of Australasian platycercine parrots d M. Schweizer et al.

Fig. 1 50% majority-rule consensus tree of the Bayesian inference using MRBAYES. Clade credibility values and bootstrap values above 50 of the maximum-likelihood inference with RAxML are indicated at each node. Platycercinae and a notation used in the text for a group within this clade are indicated to the right of the tree. Pie charts indicate at each node the support values in the separate analyses of the mitochondrial and nuclear markers for the Bayesian inference, maximum-likelihood and maximum parsimony analyses.

supported. Two trees were found to be equally parsimoni- from the 50% majority-rule consensus tree of MRBAYES in ous in maximum parsimony analyses. The strict consensus the position of Psittacella and the clade consisting of Aga- tree revealed Platycercinae to be monophyletic, but this pornis and Loriculus. Furthermore, Purpureicephalus spurius clade was not supported. The topology within this taxon clustered with Psephotus varius as in the maximum-likeli- was very similar to the Bayesian tree. However, Northiella hood tree. haematogaster and Psephotus haematonotus were the sister When the nuclear and mitochondrial markers were anal- group to the remaining ‘core platycercines’, and the posi- ysed separately using MRBAYES, the following parameter tion of Purpureicephalus spurius and Psephotus varius was not setting were chosen: different models of sequence evolu- resolved in their cluster with P. dissimilis and P. chrysoptery- tion for the two genes and three codon positions in the gius. Further, Lathamus discolor and Prosopeia formed the mitochondrial markers, and for the three genes and first sister group, the clade consisting of Eunymphicus and Cyan- and second vs. third codon position for the nuclear mark- oramphus. The topology of the BEAST tree (Fig. 2) differed ers. Compared with the combined analyses, there were a

6 ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters M. Schweizer et al. d Biogeography of Australasian platycercine parrots

Fig. 2 Maximum clade credibility tree of the dating analysis using BEAST with nodes corresponding to estimated mean ages. 95% highest posterior density (HPD) distributions are shown for the nodes in the tree that had a posterior probability >0.5. Node numbers refer to Table 4. smaller number of supported nodes in the resulting trees (95% HPD: 14.88–29.73 Ma) above the mean value of the for both data sets (Fig. 1); however, there was no conflict prior distribution. The diversification of the main clades between supported nodes. of Platycercinae started around 15 Ma in the middle Mio- cene. The mean values of the time estimates for the splits Molecular dating outside Platycercinae were found to be older (about four The comparison of the two independent runs for the millions of years, split between Loriculus and Agapornis; BEAST analyses revealed high convergence among the dif- about seven millions of years, split of Melopsittacus from ferent parameters. The two runs were then combined with Lorini) or younger (about five millions of years, split of 2.5 million generations of burn-in for each. Effective sam- Micropsitta from Psittaculini) compared to our previous ples sizes were >214 for all parameters, and the maximum study (Schweizer et al. 2011). These divergence time esti- clade credibility tree was then estimated from 50 003 mates may have been influenced by incomplete taxon sam- trees. pling outside Platycercinae. On the other hand, this Divergence time estimates dated the initial split within should not have influenced the divergence estimates for the crown group parrots at 46.54 Ma (95% HPD: 30.80– the splits within Platycercinae as these were constrained 62.82 Ma) below the mean value of our prior distribution by our prior distributions. (Fig. 2, Table 4). This is close to the results of White et al. (2011) and Pratt et al. (2009), whose mean age esti- Biogeographic reconstruction mate placed the same split at 47.4 or 50.38 Ma, respec- The global ML at the root node was )45.33 (dispersal tively, based on complete mitochondrial genomes and rate = 0.01168, extinction rate = 0.007814). The recon- external calibration points. struction of the biogeographic history for each node, based The initial split within Platycercinae occurred at on the split between areas with the highest likelihood, 30.96 Ma (95% HPD: 20.43–41.43), while the diversifica- found the origin of Platycercinae in the Bassian province. tion of the ‘core platycercines’ started around 22.33 Ma We revealed that the Eyrean province was colonized six

ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters 7 Biogeography of Australasian platycercine parrots d M. Schweizer et al.

Table 4 Estimated divergence dates for different nodes using the be a sign of a close phylogenetic relationship, but may Bayesian relaxed molecular clock approach of BEAST. The mean instead indicate a plesiomorphic pattern or convergent values and the 95% highest posterior density (HPD) distributions evolution. are given. Node numbers refer to Fig. 2. The nodes that were We uncovered the clade consisting of Pezoporus, Neopse- used for calibration are given in boldface photus bourkii and Neophema (Pezoporini) as the sister

Node number Mean 95% HPD (Millions of years ago) group of the remaining Platycercinae (Platycercini); how- ever, this cluster was not robustly supported. Such a rela- 1 49.54 30.80–62.82 tionship was already indicated by Schweizer et al. (2010, 2 30.96 20.43–41.43 3 22.33 14.88–29.73 2011), but Pezoporus was not included in those studies. In 4 27.65 17.91–37.26 contrast to Wright et al. (2008), we found no indication 5 22.34 14.24–30.47 for a close relationship between Pezoporini and Agapornis– 6 13.49 8.26–18.81 Loriculus. Similarly, Joseph et al. (2011) concluded that the 7 8 4.48–11.6 Pezoporini clade was most likely the sister group of the 8 16.05 10.51–21.76 9 14.09 9.2–19.38 remaining Platycercinae (Platycercini), although this rela- 10 11.32 7.11–15.61 tionship was never robustly supported in their data. The 11 5.01 2.93–7.11 phylogenetic position of Pezoporini also remains unclear 12 2.55 1.25–4.06 from morphological data (Mayr 2010); thus, more data 13 2.49 1.25–3.82 need to be analysed to robustly resolve their phylogenetic 14 1.40 0.68–2.24 15 12.29 7.73–16.9 relationship. The same is true for Psittacella: like other 16 10.64 6.63–15 molecular phylogenetic studies (Joseph et al. 2011; Schwe- 17 6.88 3.91–10.02 izer et al. 2011), we could not robustly resolve its phyloge- 18 13.18 8.34–18.31 netic position, but confirm that it has neither close affinity 19 11.45 7.05–15.97 to Psittaculinae nor to Platycercinae. 20 7.97 4.62–11.42 21 0.94 0.39–1.6 We corroborated that Lathamus discolor is not part of 22 0.22 0.03–0.47 the ‘core platycercines’ (cf. Schweizer et al. 2010, 2011; Joseph et al. 2011). The relationships within the latter group are in conflict with their current generic treatment. times from the Bassian province (Fig. 3). A derivation of Importantly, the genus Psephotus was found to be polyphy- Torresian from Bassian taxa was found twice. Colonization letic. Although with a more limited taxon sampling of Pse- of the Pacific islands first comprised dispersal from the photus, this has already been shown by Joseph et al. (2011) Bassian region to Melanesia followed by the colonization and indicated by Schweizer et al. (2011). Forshaw (1981) of New Zealand. For several nodes, alternative splits were considered Psephotus haematonotus and Psephotus varius as found within two log-likelihood units of the maximum for closely allied owing to their similar plumage patterns and each node (Table 5); however, they did not change the marked sexual dimorphism. However, we consistently general picture of dispersal and colonization events. As found P. varius in a clade with Purpureicephalus spurius and Pezoporini were not resolved with robust support values the two closely related taxa Psephotus chrysopterygius and as the sister group of Platycercini, we tested the robustness Psephotus dissimilis (2011). Although the relationships of of our biogeographic inference for the latter group. We P. haematonotus in combination with Northiella haematogas- reconstructed their biogeographic history separately or ter could not be resolved with robust support throughout, coded the range of a potential sister group as Tumbunan they were found to be closer related to Platycercus and to account for the probability that a sister group of Platy- Barnardius than to the clade consisting of the other cercini occurred in a rainforest habitat. However, this did Psephotus species and P. spurius. Joseph et al. (2011) could not influence the inferred biogeographic pattern for Platy- neither robustly resolve the position of P. haematonotus cercini. (and N. haematogaster), but in congruence with our results, it never clustered with the remaining Psephotus species Discussion analysed there (P. dissimilis, P. varius). Phylogenetic relationships The revealed relationship of P. spurius is remarkable. It The phylogenetic relationships within the ‘core platycer- differs from the remaining Platycercinae among others by cines’ revealed in this study are in some cases in contradic- a narrow projecting bill and by a narrowing of the anterior tion with traditional thinking and taxonomic treatment, of the cranium (Forshaw 1981). Early authors have placed which is mainly based on non-molecular traits. We espe- it near Platycercus and Barnardius (e.g. Finsch 1867; Salva- cially show that shared plumage features may not always dori 1891) or even together with Eunymphicus (Cain 1955),

8 ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters M. Schweizer et al. d Biogeography of Australasian platycercine parrots

Fig. 3 Biogeographic reconstruction of the area splits at the different nodes within Platycercinae. Only the most likely splits are shown, and node numbers refer to Table 5. The different biogeographic provinces are represented in different colours. The beginning of the aridification is indicated on the timescale at the bottom of the tree. Numbers in black circles illustrate hypothesized vicariance and long- distance dispersal events. 1: Torresian ⁄ Bassian divergence. 2: east ⁄ west Bassian divergence. 3: divergence across Carpentarian faunal barrier. 4: colonization of Melanesia from Bassian region. 5: colonization of New Zealand from Melanesia. while Homberger (1980) described similarities in the audi- (2011) and this study, an assembly of all ‘core platycer- tory region of the skull between Purpureicephalus, Psephotus cines’ in the genus Platycercus under priority rules would and Barnardius. be the best solution in order to avoid the creation of Generic treatment will certainly have to be revised in multiple phylogenetically uninformative monotypic gen- the ‘core platycercines’; however, before the relation- era. Although the positions of N. haematogaster and ships between N. haematogaster and P. haematonotus are P. haematonotus were not robustly supported, the two consistently resolved, we refrain from proposing any clades within the ‘core platycercines’ indicated in our provisional revision. Based on the results of Joseph et al. study could also support a division into the two genera

ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters 9 Biogeography of Australasian platycercine parrots d M. Schweizer et al.

Table 5 Biogeographic reconstruction with Lagrange for the Biogeography, spatial and temporal diversification patterns different area splits within Platycercinae. All reconstructions The mesic biome was confirmed as the ancestral area of within two log-likelihood units of the maximum for each node are Platycercinae. According to our biogeographic reconstruc- shown, with Rel. Prob. being the relative probability (fraction of tion, the group has its source of diversity in the Bassian the global likelihood) of a split. The numbering of the nodes corresponds to Fig. 3. The split format reads as follows: biota and seems to have originated there around 32 Ma. [left|right], where ‘left’ and ‘right’ are the ranges inherited by All dry-adapted Eyrean platycercine parrots, the Torresian each descendant branch with ‘left’ corresponding to the upper as well as the Melanesian and New Zealand taxa thus branch and ‘right’ to the lower branch in the phylogenetic tree in derive from Bassian ancestors (cf. Christidis et al. 1991; Fig. 3 Schodde 2006). The mesic biomes of the northern, eastern and southern coastline of Australia today were more wide- Node Split lnL Rel. Prob. spread until the mid-Tertiary and stem from the ancestral 1 [Bas|Bas] )46.26 0.3957 Mesozoic Gondwanan forests (Schodde 2006). The Austra- [Bas + Ey|Bas] )46.77 0.2366 lian landscape only changed during the Neogene from one ) [Bas|Bas + Mel] 47.34 0.1335 dominated by rainforest to one dominated by open vegeta- 2 [Bas|Bas] )45.91 0.5603 tion. Present-day communities had developed to some [Ey|Bas + Ey] )47.64 0.09969 [Bas|Bas + Ey] )47.64 0.09969 degree only by the end of the Pliocene with subsequent [Bas + Ey|Bas] )47.85 0.08065 major changes during the Pleistocene (Kershaw et al. 3 [Bas|Bas] )46.2 0.4171 1994), and ever-wet forests are now restricted to small scat- ) [Bas|Ey] 46.34 0.3632 tered areas along the east coast (Byrne et al. 2011). [Bas|Bas + Ey] )47.71 0.09304 Although no platycercine parrots occur in the rainforest 4 [Bas|Bas] )45.4 0.9361 5 [Bas|Bas] )45.35 0.9835 remains of Australia today, we cannot exclude that this was 6 [Bas|Bas] )45.98 0.5248 the case when this biome was more widespread in the past. [Bas + Mel|Bas] )46.79 0.2323 There is evidence that rainforest communities suffered ) [Bas|Bas + Ey] 47.68 0.09498 extinction during the Neogene (Byrne et al. 2011), and this 7 [Bas|Mel] )45.61 0.7569 may have also been the case in platycercine parrots. 8 [Mel|Mel] )45.52 0.827 9 [NewZ|Mel] )45.76 0.652 The divergence between the ‘core platycercines’ and the [Mel|Mel] )46.79 0.231 last common ancestor of Lathamus, Prosopeia, Eunymphicus 10 [NewZ|NewZ] )45.34 0.99 and Cyanoramphus took place in the beginning of the Mio- ) 11 [Mel|Mel] 45.33 0.9964 cene around 23 Ma. Both groups started only to diversify 12 [Bas|Bas] )45.96 0.5351 from middle Miocene onwards coinciding with the begin- [Bas|Bas + Ey] )46.84 0.2214 [Tor + Bas|Bas] )46.96 0.1965 ning of severe aridification in Australia (Kershaw et al. 13 [Tor|Bas] )45.69 0.699 1994; Jacobs et al. 1999; Martin 2006; Byrne et al. 2008). [Bas|Bas] )46.99 0.1907 Thus, early divergence within Platycercinae and the radia- ) 14 [Tor|Tor] 45.47 0.8683 tion of the ‘core platycercines’ occurred earlier than pro- 15 [Bas|Bas] )45.41 0.9225 posed by Christidis et al. (1991). 16 [Bas|Bas] )45.81 0.6161 [Ey|Bas] )46.75 0.2418 The Eyrean taxa that occupy the dry areas of Australia 17 [Bas|Bas] )45.43 0.9032 were not found to cluster together and were all indepen- 18 [Bas|Bas] )45.5 0.8442 dently derived from Bassian ancestors. We thus found no ) [Bas + Ey|Bas] 47.5 0.1146 indication for speciation within the arid zone, although we 19 [Bas|Bas] )46.82 0.2248 cannot exclude that arid lineages went extinct especially [Bas + Ey|Ey] )46.99 0.1898 [Ey|Bas + Ey] )46.99 0.1898 during the dramatic climate changes of the Pleistocene (cf. [Bas + Ey|Bas] )46.99 0.1898 Byrne et al. 2008). The lineage of the strictly Eyrean taxa [Bas|Bas + Ey] )46.99 0.1898 Neopsephotus bourkii split rather early from its closest rela- ) 20 [Bas|Bas] 45.67 0.7149 tive (Neophema) in the late Oligocene ⁄ early Miocene [Bas|Tor + Bas] )46.63 0.2717 (around 24 Ma). This divergence occurred before the onset 21 [Bas|Bas] )45.33 0.9986 22 [Bas|Tor] )45.36 0.9693 of the aridification of Australia, and N. bourkii may have adapted to arid landscapes in situ. In contrast, Northiella ha- ematogaster became a separate evolutionary lineage in the Platycercus (including Platycercus, Barnardius, Psephotus middle Miocene (around 16 Ma) contemporaneous with haematonotus and Northiella haematogaster)andPurpurei- the start of severe aridification. Other arid-adapted lineages cephalus (including the remaining Psephotus species and within Platycercinae concern Psephotus varius and both Purpureicephalus spurius). Barnardius species. They not only occur in Eyrean, but also

10 ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters M. Schweizer et al. d Biogeography of Australasian platycercine parrots in Bassian biota and colonized arid biota from there with- (Cracraft 1986; Schodde 2006; Bowman et al. 2009), and out subsequent speciation. However, there is evidence for temporal patterns of disjunctions along it were found to differentiation along a forest to dry open habitat environ- be rather variable. In two honeyeater species, they ranged mental gradient in Barnardius (Joseph & Wilke 2006). We from around 4 Ma (Melithreptus albogularis) to around found the divergence between the two Barnardius species 0.7 Ma (M. gularis) (Toon et al. 2010), while grassfinch to have occurred around 3 Ma in accordance with Joseph species (Poephila cincta and P. acuticauda ⁄ hecki) diverged at & Wilke (2006), who inferred that ancestral populations of 0.6 Ma (Jennings & Edwards 2005) and divergence times the Barnardius complex were first split at around 2 Ma around 0.27 Ma were estimated in the Fairy Wren Malu- based on data of the mitochondrial ND2 gene. They pro- rus melanocephalus (Lee & Edwards 2008). This rather high posed that vicariance across the Eyrean barrier could have variation in the temporal divergence between taxa on caused this divergence. This barrier marks the division either side of the Carpentarian barrier seems to reflect a between eastern and western Bassian and Eyrean biota at long and dynamic history influenced by Plio-Pleistocene the head of Spencer Gulf (Joseph & Wilke 2006; Schodde climatic cycles and different ecological conditions with 2006). An east–west Bassian disjunction is also apparent varying influences on taxa with different niches and habitat between Neophema splendida and N. pulchella. However, the requirements (Bowman et al. 2009; Toon et al. 2010). split between these two taxa occurred earlier around 8 Ma A common ancestor of Prosopeia, Eunymphicus and Cyan- during a period of major climate change termed the ‘Hill oramphus split from the Bassian taxon Lathamus discolor at Gap’ (Byrne et al. 2008). This interval, which lasted from around 14 Ma and colonized Melanesia and later New 10 to 6 Ma, marked the beginning of extreme aridity in Zealand. L. discolor is one of very few migratory parrots central Australia (Byrne et al. 2008). today (Collar 1997). If a migratory behaviour or a predis- Purpureicephalus spurius is restricted to south-west Aus- position for it was already present in the common ancestor tralia where it inhabits a variety of wooded habitats and is of this clade, this could have greatly facilitated dispersal closely associated with marri Eucalyptus calophylla (Forshaw and colonization (Joseph et al. 2011). The genus Prosopeia 1981; Schodde 2006). South-west Australia is rich in ende- is restricted to Fiji and Tonga (Collar, 1997) and forms mic taxa and recognized as a global biodiversity hotspot the sister taxon to Eunymphicus and Cyanoramphus. While (Myers et al. 2000; Hopper & Gioia 2004). Schodde the former occurs on New Caledonia, the latter is distrib- (2006) hypothesized that P. spurius became isolated in uted throughout the South Pacific including New Caledo- drier glacial times during the Quaternary when forests nia (Collar 1997). While Mayr (1939) proposed that became isolated in refugial pockets there. Such a scenario Prosopeia has a Papuan origin, Rinke (1989) considered it has been found in cockatoos, where the south-western as the only New Zealand element in the resident Fijian endemic species Calyptorhynchus baudinii and C. latirostris avifauna. In contrast, our reconstruction revealed Prosopeia split from the eastern species C. funereus at around 1.3 Ma to be of Australian origin. Most other species of the Fijian (White et al. 2011). However, we found that P. spurius avifauna are thought to have originated in Papua, while split from Psephotus varius already in the middle Miocene the few Australian taxa are considered as recent immi- around 11 Ma and the isolation of P. spurius may have grants (Mayr 1939). Prosopeia clearly is derived from an rather been caused by the expansion of arid landscapes in Australian stock; however, the taxon may have once been this time period (Kershaw et al. 1994; Jacobs et al. 1999; more widely distributed in the region and we cannot Martin 2006; Byrne et al. 2008). exclude that it also occurred in New Guinea. The region The separation of the Torresian ‘Psephotellus’ taxa (Pse- of Melanesia has a complex tectonic history (cf. Hall 2002) photus chrysopterygius and P. dissimilis) from the Bassian and New Guinea existed in separated fragments north of Pesphotus varius and Purpureicephalus spurius occurred at Australia at the beginning of the Miocene and began to around 13 Ma. The divergence of the last common ances- form its present state only 4–5 Ma (Schodde 2006). Inter- tor of these taxa into a northern and southern form may mittent land connections along the Melanesian arc could have coincided with the contraction and fragmentation of have facilitated dispersal between New Guinea and Fiji mesic biomes at this time and the development of separate (Irestedt et al. 2008; Jonsson et al. 2010). northern and southern parts of sclerophyll habitats into While Fleming (1980) proposed that New Zealand was Torresian and Bassian biota (cf. Schodde 2006). The dis- the centre of origin and dispersal in Cyanoramphus, we found tribution areas of Psephotus chrysopterygius and P. dissimilis it to have its origin in New Caledonia in congruence with are divided by the Carpentarian faunal barrier, and their other studies (Boon et al. 2001; Chambers et al. 2001). Cyan- split occurred in the late Miocene or early Pliocene at the oramphus may have dispersed to New Zealand, probably via end of the ‘Hill Gap’. The Carpentarian barrier or gap Norfolk Island, after having diverged from Eunymphicus in acted as a serial barrier to trans-Torresian connections New Caledonia (Chambers et al. 2001). The New Zealand

ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters 11 Biogeography of Australasian platycercine parrots d M. Schweizer et al. avifauna is generally most closely related to that of Australia taxa Northiella haematogaster which split from its closest (Trewick & Gibb 2010), but the Melanesian island group of relatives when the aridification of Australia started. The New Caledonia has recently been described as a major other Eyrean taxa apparently adapted to dry environments source of different taxa dispersing to New Zealand. A close after they had become separate evolutionary lineages either biogeographic connection between New Zealand and New in situ (Neopsephotus bourkii) or probably by colonization of Caledonia could also be found in geckos and different gen- arid habitats from Bassian biota without subsequent speci- era of cicadas (Chambers et al. 2001; Heads 2010). While ation (Psephotus varius, Barnardius). The diversification the biogeographic patterns observed in the geckos seem to events within non-Eyrean platycercine parrots seem to have been caused by vicariance, the cicada apparently colo- have been primarily caused by vicariance because of habi- nized New Zealand by over-water dispersal or via intermit- tat fragmentation on continental Australia following the tent land connections (Chambers et al. 2001). Although spread of arid environments or after the colonization of Heads (2010) argued that the origin of Cyanoramphus could islands in the Pacific. The lack of temporal congruence be explained by vicariance, our time estimates support the not only between potential vicariance, but also between hypothesis of Chambers et al. (2001) that Cyanoramphus colonization events implies a dynamic history with varying must have colonized New Zealand via over-water dispersal. influences on different groups. New Zealand and the New Zealand was long separated from Australia when the South Pacific were colonized by platycercine parrots not diversification of Platycercinae started in the middle Mio- directly from Australia, but via dispersal over several small cene (Trewick & Gibb 2010) and possible island chains Melanesian islands acting as stepping stones. Thus, con- which could have facilitated dispersal from New Caledonia trary to traditional biogeographic paradigms, we provide to New Zealand in the early and middle Miocene (Herzer further evidence that the colonization of oceanic islands et al. 1997; Chambers et al. 2001) predated the split between may not just be considered as one-way journeys. Eunymphicus and Cyanoramphus. It has to be taken into account that current endemic lin- Acknowledgements eages may not have evolved in the area where they are We especially thank the Silva Casa Foundation for finan- found today and may have been more widely distributed cial support of this work. We are grateful to S. Birks (Uni- in the past (Goldberg et al. 2011). This can influence the versity of Washington, Burke Museum), R. Burkhard, reconstruction of colonization patterns especially among A.T. Peterson, R.G. Moyle, M.B. Robbins and A. Nyari island groups. Nevertheless, our data clearly show that the (The University of Kansas, Natural History Museum and Melanesian islands Fiji, Tonga and New Caledonia pro- Biodiversity Research Center) as well as P. Sandmeier for vided stepping stones for parrots in their colonization of kindly providing us with tissue samples. We further thank the ‘mini continent’ New Zealand. Colonization of islands the following people for valuable support: S. Bachofner, B. from continents or larger landmasses have long been con- Blo¨chlinger, L. Joseph, M. Rieger, O. Seehausen, C. sidered as one-way journeys with islands representing evo- Sherry and T. F. Wright. lutionary dead ends whose diversity is balanced between colonization, speciation and extinction (Bellemain & References Ricklefs 2008). However, in congruence with our results, Akaike, H. (1974). New look at statistical-model identification. several recent studies have provided evidence for ‘reverse Ieee Transactions On Automatic Control, AC19, 716–723. colonization’ from oceanic islands to continents and larger Bellemain, E. & Ricklefs, R. E. (2008). Are islands the end of the landmasses, suggesting that islands may contribute to the colonization road? Trends in Ecology & Evolution, 23, 461–468. Boon, W. M., Kearvell, J. C., Daugherty, C. H. & Chambers, G. build-up of biota on larger landmasses (Filardi & Moyle K. (2000). Molecular systematics of New Zealand Cyanoramphus 2005; Bellemain & Ricklefs 2008; Jonsson et al. 2010). parakeets: conservation of orange-fronted and Forbes’ parakeets. Bird Conservation International, 10, 211–239. Conclusions Boon, W. M., Daugherty, C. H. & Chambers, G. K. (2001). The The Bassian biota was found as the area of the last com- Norfolk Island green parrot and New Caledonian red-crowned mon ancestor of platycercine parrots. Their subsequent parakeet are distinct species. Emu, 101, 113–121. diversification was shaped by the aridification of Australia 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., from mid-Miocene onwards and by long-distance coloni- Isagi, Y., Joseph, L., McBride, J., Nelson, G. & Ladiges, P. Y. zation of islands in the Pacific. The independent deriva- (2009). Biogeography of the Australian monsoon tropics. Journal tion of Eyrean lineages from Bassian ancestors did not of Biogeography, 37, 201–216. result in a radiation within the arid zone. Ecological speci- Brown, J. M. & Lemmon, A. R. (2007). 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