Molecular systematics of two enigmatic genera Psittacella and Pezoporus illuminate the ecological radiation of Australo-Papuan parrots (Aves: Psittaciformes)

Molecular Phylogenetics and Evolution 59 (2011) 675–684

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Molecular systematics of two enigmatic genera Psittacella and Pezoporus illuminate the ecological radiation of Australo-Papuan parrots (Aves: Psittaciformes) Leo Joseph a,⇑, Alicia Toon a,b, Erin E. Schirtzinger c, Timothy F. Wright c a

Australian National Wildlife Collection, CSIRO Ecosystem Sciences, GPO Box 284, Canberra, ACT 2601, Australia Australian Rivers Institute, Griffith University, Nathan, Qld 4111, Australia c Department of Biology, MSC 3AF, New Mexico State University, Las Cruces, NM 88003-0001, USA b

a r t i c l e

i n f o

Article history: Received 1 October 2010 Revised 11 March 2011 Accepted 15 March 2011 Available online 29 March 2011 Keywords: Australia Australo-Papua New Guinea Parrots Pezoporus Platycercines Psittacella Systematics

a b s t r a c t The platycercine parrots of Australia, usually recognized as the Platycercinae or Platycercini, are the broad-tailed parrots and their allies typified by the rosellas Platycercus spp. Debate concerning their circumscription has most recently centerd on the position of four genera, Neophema, Neopsephotus, Pezoporus and Psittacella, the last two having never been adequately included in sequence-based analyses. We use broad taxon sampling, mitochondrial and nuclear DNA sequence data from seven independent loci (two linked mitochondrial loci and six nuclear loci), and both gene tree and species tree approaches to reconstruct phylogenies and so determine the systematic placement all four genera. Analyses of two data sets, one of 48 taxa and five loci and one of 27 taxa and the same five plus three additional loci produced broadly congruent and consistently well-resolved phylogenies. We reject placement of any of these four genera within core platycercines. Pezoporus is closely allied to Neophema and Neopsephotus. These three genera are the likely sister group to core platycercines and we advocate their recognition as a subfamily. Psittacella is the sole extant representative of a lineage that branched very early in the history of Australo-Papuan parrot fauna and is not closely related to any of the mostly south-east Asian and Indonesian psittaculine taxa with which it is more often linked. We present a revised view of the extraordinary phylogenetic, phenotypic and ecological diversity that is the adaptive radiation of Australo-Papuan parrots. Finally, our analyses highlight the likely paraphyly of Mayr’s (2008) Loricoloriinae. Crown Copyright Ó 2011 Published by Elsevier Inc. All rights reserved.

1. Introduction The parrots (Aves: Psittaciformes) are some of the world’s most familiar and recognizable birds due to their popularity in captivity, their extraordinarily conserved morphology, and, increasingly, their widespread endangerment. Anatomical characters in living and fossil parrots (osteology, myology, arterial structure) have long been used to address higher-order relationships (reviewed in Boles, 2002; Wright et al., 2008; Forshaw, 1989; Mayr, 2008, 2010). More recently, analyses of allozymes and DNA sequences have been used to clarify these relationships (see Christidis et al., 1991; de Kloet and de Kloet, 2005; Miyaki et al., 1998; Schweizer et al., 2010; Tavares et al., 2004, 2006; Wright et al., 2008). Major divisions among parrots, especially Neotropical species, are now reasonably well understood (Eberhard and Bermingham, 2005; Ribas et al., 2005; Schweizer et al., 2010; Wright et al., 2008). Here we focus on an Old World group with problematic limits, the platycercine or broad-tailed parrots of Australasia, familiarly known as ⇑ Corresponding author. Fax: +61 2 6242 1689. E-mail address: [email protected] (L. Joseph).

the rosellas and their relatives. This group is usually recognized as the Platycercinae within Psittacidae (e.g., Schodde, 1997) or Platycercini within the Psittacinae (Forshaw, 2002, 2006). There is general agreement that platycercines include the Australian endemic genera found almost exclusively in temperate forests and semi-arid woodlands. We term these genera the core platycercines: Platycercus, Barnardius, Psephotus, Northiella, Purpureicephalus, and Lathamus as well as the three genera Cyanoramphus, Eunymphicus and Prosopeia found in New Zealand and the Pacific island regions (Boon et al., 2008; Christidis et al., 1991; Condon, 1941; Homberger, 1980; Joseph et al., 2008; Mayr, 2008; Ovenden et al., 1987; Schodde, 1997; Smith, 1975). Although some early treatments of this group included the monotypic genus Melopsittacus of the arid zone (the familiar budgerigar Melopsittacus undulatus), recent analyses of both DNA sequences and morphology clearly show that it is more closely related to mostly mesic zone lorikeets and rainforest-inhabiting fig-parrots (de Kloet and de Kloet, 2005; Mayr, 2008; Schweizer et al., 2010; Wright et al., 2008). There is lingering debate over the inclusion of four other genera: Neophema (six species) Neopsephotus (one), Pezoporus (three; see Murphy et al., 2011) and Psittacella (four). Of these four

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L. Joseph et al. / Molecular Phylogenetics and Evolution 59 (2011) 675–684

genera, Neophema, Neopsephotus, and Pezoporus are found in temperate and arid Australia while Psittacella inhabits the tropical rain-forests of New Guinea. Wright et al. (2008), based on sequences from two mitochondrial loci and three nuclear introns, found robust support for Neophema and Neopsephotus being most closely related to Agapornis, Loriculus and Bolbopsittacus, which range from Africa to east of Wallace’s Line in New Guinea but not Australia (see Wright et al., 2008). Conversely, Schweizer et al. (2010) analysed sequences from three nuclear exons and found Neophema and Neopsephotus to be sister to all other platycercines but with relatively low support. From osteological evidence, Mayr (2010) also concluded that Neophema and Neopsephotus are not closely related to core platycercine genera. Relationships of Psittacella and Pezoporus, which have not been included in any previous DNA sequence study, remain especially contentious and, with Neophema and Neopsephotus, are the primary foci of the present study. Resolution of the systematics of Pezoporus and Psittacella is of particular biogeographic interest. Pezoporus comprises three species with fragmented ranges across inland and subcoastal southern Australia (Forshaw, 2002; McDougall et al., 2009; Murphy et al., 2011). Clarification of relationships within Pezoporus and identification of their closest relatives would inform how they have speciated on the Australian landscape and contribute to the broader questions of relationships among mesic and xeric biota in Australia. Their long-presumed association with Melopsittacus and the platycercines has been based on similarities in plumage pattern and nestlings’ food-begging calls, traits that have not been assessed in using independently derived phylogenies (Christidis et al., 1991; Courtney, 1997). Leeton et al. (1994) aligned Pezoporus, Melopsittacus and Neophema with Platycercus based on partial mitochondrial DNA (mtDNA) sequences but that study’s sequences were later withdrawn from GenBank. Systematics and biogeography of New Guinean Psittacella are even more poorly understood. Its placement in the Psittaculini or alternatively, treatment as platycercine, has been based on morphological traits not analysed in a phylogenetic context (Christidis et al., 1991; Forshaw, 1989; Schodde, 2006; Smith, 1975). Christidis et al.’s (1991) distance-based analyses of allozyme data could not resolve relationships of Psittacella. Based on similarities in a number of morphological characters, they considered it platycercine but of ‘‘disparate affinity’’ to that group. Resolution of the systematic position of Psittacella, and the question of whether it is platycercine, could inform a range of evolutionary and ecological topics. If platycercine, it would be the only member of that group in New Guinea and indeed in mountain rainforest habitats generally above 1100 m altitude. It could address whether the relatively slender-bodied, long-tailed morphology of platycercines is derived from stouter, short-tailed Psittacella-like ancestors and test the hypothesis that arid and semi-arid zone platycercines, which mostly feed terrestrially in Australia have been derived from montane arboreal rainforest ancestors in New Guinea (see Schodde, 1982; Schodde and Calaby, 1972). The primary aim of the present study is to clarify the limits of the platycercine parrots by including Pezoporus and Psittacella for the first time in a multilocus DNA sequence-based data set with comprehensive sampling of other platycercine parrots, including Neophema and Neopsephotus. A secondary aim is to clarify relationships within Pezoporus by testing (1) whether Murphy et al.’s (2011) recognition of Pezoporus flaviventris as a sister species to Pezoporus wallicus based on mtDNA and phenotypic data is supported by nuclear data and (2) whether Pezoporus occidentalis is in turn their sister. Lastly, we discuss implications of our findings to understanding the ecological history of parrots in the Australo-Papuan region.

2. Materials and methods 2.1. Taxon sampling Source tissues were frozen samples from vouchered museum specimens or blood from birds held in zoos for some non Australo-Papuan species. We sampled single individuals of 48 parrot taxa representing 31 Australasian genera and 7 genera from other regions (Table 1). Psittacella was represented by Psittacella brehmii and Psittacella picta, Pezoporus by Pe. occidentalis, Pe. wallicus and Pe. flaviventris. Core platycercine genera were Platycercus, Barnardius, Purpureicephalus, Northiella, Psephotus, Cyanoramphus, Eunymphicus, Lathamus, and Prosopeia. Neophema and Neopsephotus also were included to investigate their relationship to Pezoporus and the core platycercines. Other genera included as potential relatives of Psittacella (Forshaw, 2006; Smith, 1975) were Tanygnathus, Loriculus, Agapornis, Bolbopsittacus, Prioniturus, Psittacula, Micropsitta, Geoffroyus, Eclectus, Alisterus, Aprosmictus and Polytelis. New Zealand taxa Strigops and Nestor were used as outgroups (de Kloet and de Kloet, 2005; Schweizer et al., 2010; Wright et al., 2008). Nomenclature follows Forshaw (2006) except for recent species-level recognition of Pe. flaviventris based on mtDNA and morphology (Murphy et al., 2011). 2.2. Character sampling We isolated genomic DNA using DNeasy extraction kits following manufacturer’s protocols (Qiagen, Valencia CA). We sampled all taxa at two linked mitochondrial protein-coding genes [cytochrome oxidase I (COI) and NADH dehydrogenase 2 (ND2)] and three non-coding nuclear introns [tropomyosin alpha-subunit intron 5 (TROP), and transforming growth factor b-2 intron 5 (TGFB2), rhodopsin intron 1 (RDPSN)]. In addition, we sampled 27 of these taxa at three single-copy nuclear exons: the protooncogene c-mos (c-mos), recombination activating protein (RAG1) and the transcription factor ZENK, a homolog of the early growth response-1 gene (ZENK). For the mtDNA loci and nuclear introns we used primers given in Wright et al. (2008); primers for the nuclear exons were from Schweizer et al. (2010). Amplification for all loci followed protocols in Wright et al. (2008) excepting sequences from Schweizer et al. (2010) downloaded from GenBank. All amplicons were sequenced in both directions at the University of Chicago Cancer Sequencing Facility using an ABI 3730 DNA Analyzer and ABI Big Dye chemistry. We did not obtain RDPSN sequences for Barnardius barnardi, Barnardius zonarius, Coracopsis vasa, Eunymphicus uvaeensis, Pe. occidentalis, Platycercus elegans, Polytelis anthopeplus, Psephotus dissimilis, Psephotus haematonotus, Psephotus varius, Psittacella picta, and Psittacus erithacus; c-mos was not obtained for M. undulatus. Sequences were combined into a single consensus sequence using Sequencher 4.7 (Gene Codes, Ann Arbor, MI). See Table 1 for GenBank accession numbers. 2.3. Phylogenetic analysis We aligned the sequences for each gene region with Clustal W (Chenna et al., 2003) using the default parameters for gap opening and extension penalties with the exception of RDPSN where we used a gap opening penalty of 5 and an extension penalty of 2.5 to improve alignment of the terminal ends of the sequences. We combined the resulting alignments in PAUP version 4.0b10 (Swofford, 1999) to create two datasets. The ‘Primary dataset’ included 48 taxa and five loci (COI, ND2, TROP, TGFB2, and RDPSN); the ‘Secondary dataset’ included 27 taxa and three additional loci (c-mos, Rag-1 and ZENK). Previous analyses of parrot relationships employing the same five loci as in the Primary dataset detected little conflict in

Table 1 Species and loci sampled for study of evolutionary relationships of the Australo-Papuan parrot genera Pezoporus and Psittacella. Museum/collectiona

Specimen numbera

Sample typea

Agapornis roseicollis Alisterus amboinensis Aprosmictus erythropterus Barnardius barnardi Barnardius zonarius Bolbopsittacus lunulatus Calyptorhynchus banksii Calyptorhynchus funereus Chalcopsitta duivenbodei Coracopsis vasa Cyanoramphus auriceps Cyanoramphus novaezelandiae Cyclopsitta diophthalma Eclectus roratus Eolophus roseicapillus Eunymphicus uvaeensis Geoffroyus heteroclitus Lathamus discolor Loriculus galgulus Melopsittacus undulatus Micropsitta finschii Myiopsitta monachus Neophema elegans Neopsephotus bourkii Nestor notabilis Northiella haematogaster Pezoporus flaviventrisb Pezoporus occidentalis Pezoporus wallicus Platycercus adscitus Platycercus elegans Poicephalus robustus Polytelis alexandrae Polytelis anthopeplus Prioniturus luconensis Prosopeia tabuensis Psephotus dissimilis Psephotus haematonotus Psephotus varius Psittacella brehmii Psittacella picta Psittacula columboides Psittaculirostris edwardsii Psittacus erithacus Psittrichas fulgidus Purpureicephalus spurius Strigops habroptilus Tanygnathus lucionensis

NMNH NMNH NMNH ANSP ANSP NMNH ANWC NMNH NMNH LPF VU AMNH AMNH NMNH NMNH LPF AMNH ANWC NMNH NMNH NMNH NMNH NMNH ANSP NMNH NMNH ABBBS QM ANWC NMNH NMNH NMNH NMNH ANWC NMNH NMNH ANWC ANWC ANSP KUMNH AM NMNH NMNH NMSU AMNH ANSP VU NMNH

B08798 B06399 B06424 10702 ANSP10669 B03677 50042 B06460 B06396 LPF07-29 (UV) FT3310 DOT 11060 DOT 7799 B06393 B06415 LPF07-34 (UV) DOT 6635 34174 B06817 B06360 B04046 B02706 B06444 ANSP11213 B02885 B06432 230-06707 QMO32613 45982 B06434 B06370 B06395 B02887 50250 B03676 B02877 33421 34210 ANSP10641 4600 AM0.59744 B06812 B06383 987 DOT 9597 ANSP11001 CD1139 B06807

T T T T T T T T T B B T T T T B T T T T T T T T T T B, D D T T T T T T T T T T T T T T T T T T B T

GenBank accession numbersc COI

ND2

TROP

TGFB2

RDPSN

C-MOS

RAG-1

ZENK

EU621593 EU621594 EU621596 HQ316859 EU621599 EU621600 HQ316860 EU621603 EU621604 EU621608 EU621611 HQ316861 EU621612 EU621615 EU621617 EU621619 EU621622 HQ316862 EU621627 EU621629 EU621630 EU621631 EU621634 EU621635 EU621637 EU621638 HQ316863 HQ316864 HQ316865 EU621647 HQ316866 EU621648 EU621649 HQ316867 EU621650 EU621652 HQ316868 HQ316869 EU621653 HQ316870 HQ316871 EU621655 EU621656 EU621657 EU621658 EU621659 EU621663 EU621664

EU327596 EU327597 EU327599 HQ316872 EU327602 EU327603 HQ316873 EU327606 EU327607 EU327612 EU327615 HQ316874 EU327616 EU327619 EU327621 EU327623 EU327626 HQ316875 EU327631 EU327633 EU327634 EU327635 EU327638 EU327639 EU327641 EU327642 HQ316876 HQ316877 HQ316878 EU327651 HQ316879 EU327652 EU327653 HQ316880 EU327654 EU327656 HQ316881 HQ316882 EU327657 HQ316883 HQ316884 EU327659 EU327660 EU327661 EU327662 EU327663 EU327667 EU327668

EU665562 EU665563 EU665565 HQ316885 EU665568 EU665569 HQ316886 EU665572 EU665573 EU665578 EU665581 HQ316887 EU665582 EU665585 EU665587 EU665589 EU665591 HQ316888 EU665596 EU665598 EU665599 EU665600 EU665603 EU665604 EU665606 EU665607 HQ316889 HQ316890 HQ316891 EU665616 HQ316892 EU665617 EU665618 HQ316893 EU665619 EU665621 HQ316894 HQ316895 HQ378188 HQ316896 HQ316897 EU665623 EU665624 EU665625 EU665626 EU665627 EU665631 EU665632

EU660234 EU660235 EU660237 HQ316898 EU660240 EU660241 HQ316899 EU660244 EU660245 EU660250 EU660252 HQ316900 EU660253 EU660256 EU660258 EU660260 EU660263 HQ316901 EU660267 EU660269 EU660270 EU660271 EU660273 EU660274 EU660276 EU660277 HQ316902 HQ316903 HQ316904 EU660285 HQ316905 EU660286 EU660287 HQ316906 EU660288 EU660290 HQ316907 HQ316908 EU660291 HQ316909 HQ316910 EU660293 EU660294 EU660295 EU660296 EU660297 EU660301 EU660302

EU665501 EU665502 EU665504

GQ505086 HQ316816 HQ316817

GQ505194 HQ316830 HQ316831

GQ505141 HQ316844 HQ316845

HQ316818 HQ316819 GQ505113 GQ505104

HQ316832 HQ316833 GQ505223 GQ505213

HQ316846 HQ316847 GQ505167 GQ505158

GQ505135

GQ505244

GQ505187

HQ316820 GQ505102 HQ316821 GQ505128

HQ316834 GQ505211 GQ505196 HQ316835 GQ505240

HQ316848 GQ505156 HQ316849 HQ316850 GQ505182

HQ316822 GQ505112

HQ316836 GQ505221

HQ316851 GQ505165

HQ316813 EU665544

HQ316823 HQ316824 HQ316825 HQ316826

HQ316837 HQ316838 HQ316839 HQ316840

HQ316852 HQ316853 HQ316854 HQ316855

HQ316814 EU665545

GQ505093

GQ505201

GQ505147

HQ316827

HQ316841

HQ316856

GQ505101

GQ505210

GQ505155

HQ316828 HQ316829

HQ316842 HQ316843

HQ316857 HQ316858

GQ505132 GQ505115 GQ505127

GQ505243 GQ505225 GQ505239

GQ505185 GQ505168 GQ505181

EU665507 HQ316809 EU665510 EU665511 EU665516 HQ316810 EU665517 EU665520 EU665522 EU665525 HQ316811 EU665527 EU665529 EU737241 EU665531 EU665533 EU665534 EU665536 EU665537 HQ316812

EU665546 EU665548

HQ316815 EU665550 EU665551 EU665552 EU665553 EU665557 EU665558

677

a Sample information refers only to sequences obtained by Wright et al. (2008) or in the present study. Sample information for sequences obtained by Schweizer et al. (2010) is available therein. Abbreviations: ABBBS, Australian Bird and Bat Banding Scheme, Canberra; AM, Australian Museum, Sydney; AMNH, American Museum of Natural History, New York; ANSP, Academy of Natural Sciences, Philadelphia; ANWC, Australian National Wildlife Collection, Canberra; LP, Loro Parque Fundación, Tenerife, Spain; MV, Museum Victoria, Melbourne; NMNH, Smithsonian National Museum of Natural History, Washington DC; NMSU, New Mexico State University Vertebrate Museum, Las Cruces; QM, Queensland Museum, Brisbane; VU, Victoria University, Wellington. Abbreviations for sample type: T, tissue; B, blood, D, DNA extract provided by collection. b Sample obtained from live bird that was banded and released. c Accession numbers starting with HQ identify sequences obtained in this study, those starting with EU were obtained by Wright et al. (2008); those starting with GQ were obtained by Schweizer et al. (2009).

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phylogenetic signal between these loci (Wright et al., 2008). Accordingly, we used a combined phylogenetic analysis approach in which we concatenated or partitioned the five loci for searches using maximum likelihood (ML) and Bayesian (MB) criteria, respectively. For ML searches, we used the general time reversible model plus invariant sites and a gamma distribution (GTR + I + G) model selected by the Akaike Information Criteria (AIC) in ModelTest 3.8 (Posada, 2006). The ML heuristic search was conducted in PAUP using a random starting topology, TBR branch swapping, and proportion of invariant sites of 0.2944 and gamma shape distribution of 0.51. Nodal support was assessed with 100 bootstrap replicates in GARLI version 0.951 (Zwickl, 2006) using the same ML model, random starting trees and default parameters for the genetic search algorithm. For the MB searches, we used MrModelTest version 2.0 (Nylander, 2004) to select the best fit model under the AIC for each of the five gene regions (Table 2). We tested whether to partition by codon within the mtDNA coding gene regions by partitioning each region using first, second and third positions then comparing with a non-partitioned gene dataset using Bayes factor analysis (Nylander, 2004). Analyses were run in MrBayes version 3.1.2 (Ronquist and Huelsenbeck, 2003) and the harmonic mean of the estimated likelihood for nested analyses were compared. Partitioning of the mtDNA gene regions (ND2, COI) by codon was strongly supported by the Bayes factor and used in further analysis (Table 2). We also included indels as characters using the simple gap coding method following Simmons and Ochoterena (2000) and implemented in SeqState 1.4.1 (Müller, 2005). We then used a Bayesian framework with Markov chain Monte Carlo (MB) inference to estimate phylogenies using a dataset of five gene regions plus coded gaps. The MB analysis was run in MrBayes version 3.1.2 (Ronquist and Huelsenbeck, 2003) with 1  107 generations sampled every 1000 generations. All analyses were run on the CIPRES 2.0 portal (Stamatakis et al., 2008) and the Computational Biology Service Unit from Cornell University. Each analysis was run three times starting from random trees. Convergence and mixing was assessed for all the parameters in Tracer 1.4 (Drummond and Rambaut, 2007). Each run was also evaluated for stationarity by comparing log-likelihood values over time and 10% of generations (1  106) were discarded as burn-in. The posterior probabilities for individual clades obtained from separate analyses were compared for congruence and then combined and summarized on a 50% majorityrule consensus tree (Huelsenbeck and Imennov, 2002; Huelsenbeck et al., 2002). Based on results from these initial searches with the Primary dataset, we refined our analysis by reducing the number of taxa to 27 and adding three additional loci in order to focus on clades of particular interest and improve resolution at basal nodes of the trees (Table 1). We analyzed this Secondary dataset with MB

searches using the eight gene regions plus coded gaps as separate partitions. As with the Primary dataset, partitioning by codon was strongly supported for the mtDNA gene regions (ND2, COI) and was used in further analyses; partitioning of the nDNA by codon was not supported and was not employed in further analyses (Table 2). MB analyses were conducted on the entire concatenated dataset of eight gene regions and also on the mtDNA gene regions and nuclear gene regions separately to assess conflict between the nuclear and mitochondrial loci. We also implemented the species tree approach in BEST (Liu, 2008) to incorporate gene tree heterogeneity (Edwards, 2008; Liu and Edwards, 2009). The Best analysis was run in mbbest (Liu, 2008), in MrBayes (Ronquist and Huelsenbeck, 2003) at the Computational Biology Service Unit at Cornell University. Two analyses were run, one with the combined mtDNA and nDNA, and one with nDNA gene regions only. Model parameters estimated from ModelTest were included as unlinked partitions for each gene region. Initially we used priors suggested in the manual (inverse gamma distribution (3, 0.003) for theta and a uniform distribution (0.2, 2) for gene mutation) but our searches were unable to reach convergence. We did reach convergence by selecting a broader inverse gamma distribution prior (1, 1) (Wiens et al., 2010). We sampled every 1000 generations for 2  107 generations. Convergence and mixing was assessed for all the parameters in Tracer v1.4 (Drummond and Rambaut, 2007). Species trees were constructed from combined runs. 3. Results 3.1. Sequence characteristics Sequences obtained for the mtDNA genes were consistent in length across all 48 taxa: 570 base pairs (bp) for COI and 1041 bp for ND2. No stop codons or frameshift mutations were detected, suggesting that sequences were mitochondrial in origin and not nuclear pseudogenes. In contrast, sequence lengths were more variable in the three nuclear intron loci. Across the 48 taxa sampled, TROP sequences varied from 518 to 540 bp, TGFB2 sequences varied from 610 to 628 bp, and RDPSN sequences varied from 732 to 795 bp in length. The three nuclear coding regions, which were only sampled for the 27 taxa in the Secondary dataset, showed intermediate levels of length variation, with C-MOS sequences ranging from 600 to 603 bp, RAG-1 sequences ranging from 1449 to 1458 bp, and ZENK sequences ranging from 1137 to 1146 bp in length. No unexpected stop codons were detected and all indels were of entire codons. After alignment and concatenation, the Primary dataset was 3622 bp in length plus 100 coded gap characters and the Secondary dataset was 6803 bp in length plus 79 coded gap characters (Table 2).

Table 2 Model and partition data for each gene region included in the phylogenetic analyses. Dataset

Gene region

Aligned characters

Model

Partition

Primary (48 Taxa)

COI ND2 TROP TGFB2 RDPSN Concatenated

570 1041 548 646 817 3622

GTR + I + G GTR + I + G GTR + G HKY + G HKY + G GTR + I + G

Codon Codon Gene region Gene region Gene region Entire alignment

Secondary (27 Taxa)

COI ND2 c-mos RAG1 ZENK TROP TGFB2 RDPSN

570 1041 603 1458 1146 536 639 810

GTR + I + G GTR + I + G GTR + I + G GTR + I + G GTR + I + G GTR + G HKY + G HKY + G

Codon Codon Gene region Gene region Gene region Gene region Gene region Gene region

L. Joseph et al. / Molecular Phylogenetics and Evolution 59 (2011) 675–684

3.2. Phylogenetic analysis For the Primary dataset, the ML analysis produced a single tree with a score of 32,914 that exhibited broad congruence with the majority consensus tree recovered using the MB analysis (Fig. 1). The ML and MB trees for the Primary dataset were consistent in showing monophyly of Pezoporus, with strong support for a clade of Pe. wallicus and Pe. flaviventris, which was in turn sister to Pe. occidentalis. Divergence between Pe. wallicus and Pe. flaviventris was 3.0 % and that between this pair and Pe. occidentalis was

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6.1% (uncorrected p distances using mtDNA only). Also strongly supported was a clade comprising Neophema–Neopsephotus–Pezoporus, which was in turn sister to a clade comprising Agapornis–Loriculus– Bolbopsittacus, albeit with slightly lower support values. We term the clade uniting all of these taxa in analyses of the Primary dataset ‘Clade 1’. The core platycercines formed ‘Clade 2’. Strongly supported as sister to Clades 1 and 2 was ‘Clade 3’, which comprised the lorikeet-fig-parrot-budgerigar assemblage (Melopsittacus, Chalcopsitta, Cyclopsitta, Psittaculirostris). Finally, Psittacella comprised ‘Clade 4’ and was sister to Clades 1, 2 and 3 (Fig. 1).

Fig. 1. Phylogenetic reconstruction of relationships of the Australo-Papuan parrots using the Bayesian criteria and the 48 taxa and five loci used in the Primary dataset. Posterior probabilities are indicated first followed by bootstrap support values from 100 maximum likelihood runs. Values of 1.0 or 100% are indicated with asterisks; values below 0.7 or 70% are not shown. Taxa names are colored by distribution: Australia in blue, New Guinea, Indonesia east of Wallace’s Line and the south-west Pacific in purple, New Zealand in black, Africa, Madagascar and south-east Asia west of Wallace’s Line in red, and South America in yellow.

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Bayesian analyses of the Secondary dataset recovered some similar and some critically different relationships according to which loci were used. Analyses of all eight loci and of the nuclear loci alone produced a well-resolved topology, and higher nodal posterior probabilities than the Primary dataset (Fig. 2). Analysis using mtDNA recovered similar relationships among closely related species but had poor resolution at deeper nodes. The key difference in these results relative to the Primary dataset was that Agapornis–Loriculus was sister to Clade 3 whereas Pezoporus, Neophema and Neopsephotus formed a well-supported clade (Fig. 2) that was sister to the core platycercines. In all of the Secondary dataset’s analyses, Psittacella tended to be sister to this entire assemblage; the exception was in analysis of mtDNA plus nuclear coding genes in which it was sister to what we term the expanded platycercines: core platycercines + Pezoporus, Neophema and Neopsephotus. The mtDNA plus nuclear intron analysis agreed with the Primary dataset in recovering Clade 1. Examination of individual gene tree topologies in the Primary dataset suggested that recovery of Clade 1 was being driven primarily by the nuclear intron RDPSN (Supplementary material Figs. S1–S6). In each analysis there is a different relationship among Aprosmictus, Polytelis and Alisterus although none have high posterior probabilities and none impact our central focus on platycercines, Pezoporus and Psittacella. The species tree analysis using BEST achieved good mixing and convergence but, in contrast to the Bayesian analysis, showed poor resolution for both the entire dataset and for nDNA only (Supplementary material, Fig. S7). In summary, the trees obtained using the Primary and Secondary datasets supported the monophyly of Pezoporus and the sister relationship between this genus and Neophema and Neopsephotus. They differed, however, in whether this clade was sister to the clade containing Agapornis and Loriculus. In the Primary dataset all these taxa were combined in Clade 1 of Fig. 1. In the Secondary dataset, however, (1) Agapornis and Loriculus were sister to Clade 3 and (2) the clade of Pezoporus, Neophema and Neopsephotus was sister to core platycerines. None of the analyses on either dataset recovered a sister relationship of Pezoporus with Melopsittacus, or of Agapornis and Loriculus with Micropsitta. Sister taxon relationships of Psittacella could not be determined confidently in any analysis other than to infer it as sister either to the entire assemblage represented by Clades 1, 2 and 3 or, in one analysis, as sister to expanded platycercines. No analysis included either Pezoporus or Psittacella within the core platycercine clade nor were they ever found to be sister to any of the genera typically classified in the tribes Polytelini (Alisterus, Aprosmictus, Polytelis, the last named not being monophyletic as Schweizer et al., 2010 also found) or Psittaculini (Tanygnathus, Eclectus, Geoffroyus, Psittacula, Prioniturus). The latter two clades were consistently found to be monophyletic clades and sister to each other.

4. Discussion We set out to clarify the limits of platycercine (broad-tailed) parrots by determining whether two genera, Pezoporus of Australia and Psittacella of New Guinea, are closely related to core platycercine genera (Platycercus, Barnardius, Psephotus, Northiella, Purpureicephalus, Lathamus, Cyanoramphus, Eunymphicus and Prosopeia). Both Pezoporus and Psittacella have been associated with Australian platycercine parrots in distance-based analyses (see Section 1), but to date no phylogenetic analysis has adequately tested either hypothesis. We also sought to clarify relationships within Pezoporus, an enigmatic and little known genus of Australian parrots. Our results show that Psittacella is not closely aligned to the core platycercines. The composition of Pezoporus is clarified and we affirm its close relationship to, but not within, core platycercines.

Based on these results, we describe below a rigorous phylogenetic and biogeographic circumscription of platycercine parrots and consider the evolutionary history of the Australo-Papuan parrot radiation. 4.1. Systematics of Psittacella For Psittacella, we confidently reject that it is a core platycercine or, for that matter, that it is close to any of the other genera with which it has been associated in the Psittaculini (Forshaw, 2006; Smith, 1975). Almost all analyses placed it on a long branch arising early in the history of a broad, predominantly Australian assemblage comprising core platycercines (Clade 2) and a diversity of other groups including Clade 3 as well as Pezoporus, Neophema and Neopsephotus. Only one analysis recovered it as sister to an expanded platycercine assemblage that included Pezoporus, Neophema and Neopsephotus. Furthermore, we found no support for aligning it with psittaculine groups with which it has more often been placed. We acknowledge that we have only examined the two larger species of Psittacella, having been unable to locate any tissue samples of the two smaller species. Determining the systematic position of Psittacella is fundamental to understanding the biogeography and ecology of AustraloPapuan parrots. Christidis et al. (1991) confidently considered Psittacella as platycercine but with ‘‘disparate affinity’’ to the group. To reconcile their view with ours, we more closely examine the details of the earlier study’s findings. First, Christidis et al. (1991) found that a UPGMA phenogram and distance Wagner tree, both built on allozyme-based genetic distances, aligned Psittacella with core platycercines (and in one case with Pezoporus). In contrast, their consensus trees generated using parsimony criteria and the allozyme data could not resolve its position. Second, they enumerated in some detail morphological traits Psittacella shares with some but not all platycercines (e.g., blue cheek patches of Ps picta and red undertail-coverts of all Psittacella species). Given that their Wagner tree and our results at least agree in placing Psittacella well outside, not within, core platycercines, we ascribe these morphological similarities to convergence or retention of ancestral, plesiomorphic traits. Further, their earlier distance analyses were likely ill-suited to clarifying relationships at the appropriate phylogenetic depths. In summary, no previous analysis has appreciated Psittacella’s likely systematic position and biogeographical significance. Far from being a New Guinean representative of the primarily south-east Asian and Indonesian psittaculine parrots, it is an extant representative in New Guinea of a very early branch in a major radiation of Australo-Papuan parrots including platycercines and Clade 3, the lorikeet-fig-parrot-budgerigar assemblage. 4.2. Systematics of Pezoporus: species level corollaries The extreme rarity of all populations of Pezoporus precluded sampling of multiple individuals of the three relevant taxa. With that caveat, we find strong support for a sister group relationship between eastern and western populations of the ground parrot (Pe. wallicus sensu lato) and that Pe. occidentalis is their sister taxon. Our findings are consistent with Murphy et al.’s (2011) species-level recognition based on mtDNA and phenotype of Pe. wallicus (eastern ground parrot) and Pe. flaviventris (western ground parrot). Whereas adults are typically sedentary, data from juveniles of eastern populations of Pe. wallicus indicates their capacity to disperse up to 80 km (reviews in Higgins, 1999; Forshaw, 2002). Thus dispersal may have been important in the group’s evolutionary history. We suggest, however, that when viewed against the broader topography and biogeography of the Australian continent, the evolution of Pezoporus is most simply explained by sequential vicariance, first between the arid and coastal zones leading to the

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Fig. 2. Phylogenetic reconstruction of relationships of the Australo-Papuan parrots using the Bayesian criteria and the 27 taxa and eight loci used in the Secondary dataset. Posterior probabilities are indicated above branches; values of 1.0 or 100% are indicated with asterisks and values below 0.7 or 70% are not shown. Images of birds painted by Frank Knight reproduced with permission (see Acknowledgments). The species depicted, from top to bottom are shown approximately to scale, and are: Pezoporus flaviventris, Neophema elegans, Psephotus dissimilis, Melopsittacus undulatus, Loriculus galgulus, Psittacella brehmi, Eclectus roratus (male, left and female, right), Micropsitta finschii.

evolution of Pe. occidentalis and the ancestor of Pe. wallicus + flaviventris, respectively, and later within coastal zones of southern Australia, leading to Pe. wallicus and Pe. flaviventris. While recognizing current debate over the calibration of rates of molecular evolution (e.g., Lovette, 2004; Ho, 2007), we note that the conventional calibration for mtDNA evolution of 2% per million years (Tarr and Fleischer, 1993) would suggest that the split between Pe. occidentalis and Pe. wallicus/Pe. flaviventris likely occurred about 3.3 mya, certainly before the Pleistocene. Assignment of Pe. occidentalis to monotypic Geopsittacus Gould, 1861(Brereton, 1963;

Courtney, 1997; Forshaw, 1969) though not a recent practice (Forshaw, 2002, 2006; Schodde, 1997) is a valid taxonomic option consistent with our data. We see no strong imperative or justification for the use of Geopsittacus, however: it would still be sister to Pe. wallicus + Pe. flaviventris and it is not especially divergent from them relative to many other congeneric sister taxa in birds (e.g., reviews in Avise and Walker, 1998; Johnson and Cicero, 2004; Joseph and Omland, 2009; Klicka and Zink, 1997; Zink and Barrowclough, 2008). We advocate retention of Pezoporus as the simplest means of expressing the relationship of these three species to each other

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and the likely history of simple vicariance events in their group’s evolution. 4.3. Systematics of Pezoporus and limits of the platycercine parrots At the generic level, we reject a close relationship between Pezoporus and Melopsittacus. Pezoporus is, however, firmly allied as sister to Neophema and Neopsephotus. The main uncertainty in our findings concerns how closely related Pezoporus–Neophema–Neopsephotus are to the clade containing Agapornis, Loriculus and Bolbopsittacus. The linkage of Pezoporus–Neophema–Neopsephotus to non-Australian but stouter bodied Agapornis, Loriculus and Bolbopsittacus came from analyses of our Primary dataset and was apparently driven mostly by a single locus, the nuclear intron RDPSN. This result accords with Wright et al. (2008), who found similar results using the same five loci as our Primary dataset but without sampling Pezoporus. In contrast, Schweizer et al. (2010), also without sampling Pezoporus, found weak support for Neophema and Neopsephotus as sister to the core platycercine group using the three nuclear coding genes we added into our Secondary dataset. Results from our Secondary dataset were consistent with those of Schweizer et al. (2010), with Neophema–Neopsephotus as sister to the core platycercines and Agapornis–Loriculus as sister to the robustly supported Clade 3 (Melopsittacus–Chalcopsitta–Psittaculirostris) group. Accordingly, we consider the implications to the circumscription and evolution of platycercines of these two alternative placements of Agapornis–Loriculus–Bolbopsittacus. If affirmed, the radiation identified as Clade 1 from analyses of our Primary dataset (Pezoporus–Neophema–Neopsephotus–Agapornis–Loriculus–Bolbopsittacus) would entail extraordinary ecological, biogeographical and phenotypic diversity. Its geographic range would span either side of Wallace’s Line. Its habitats would include rainforest, rocky coastlines, and extremely arid and climatically unpredictable Australian deserts and African savannas. Lastly, the phenotypic diversity in plumage patterning and morphology is extreme. In contrast, if Pezoporus, Neophema and Neopsephotus (itself a group with great phenotypic diversity; Fig. 2) are the sister group to the core platycercines as in analyses of our Secondary dataset, then the platycercine radiation would be biogeographically cohesive within Australia and the Pacific, and it would have two broadly divergent subclades (core platycercines and Pezoporus–Neophema– Neopsephotus). 4.4. Evolution of Australo-Papuan parrots: closing remarks We conclude that Pezoporus–Neophema–Neopsephotus is most likely the sister group to the core platycercines. An alternative placement was supported largely by a single nuclear intron and presents a biogeographic anomaly. We advocate continued restriction of the term platycercine and its formal nomenclatural corollaries (Platycercinae, Platycercini) to the genera in Clade 2. One subclade of these core platycercines (Platycercus, Barnardius, Purpureicephalus, Psephotus, Northiella) is exclusively Australian. Their ecological radiation spans rainforest, wet temperate forests, temperate, semi-arid and monsoonal woodlands and even arid, desert shrublands. The other subclade includes three genera (Cyanoramphus, Eunymphicus, Prosopeia) that have colonized deep into the temperate and tropical south-west Pacific Ocean. Notably, their sister, monotypic Lathamus of temperate south-eastern Australian woodlands (present study; Schweizer et al., 2010), is migratory. If its migration evolved as early in the subclade’s history as the Lathamus lineage itself, then this subclade may have been predisposed to the dispersal and colonization that has clearly occurred in its history. It would represent an additional trans-oceanic dispersal event in parrots (Schweizer et al., 2010). For the robustly

supported Pezoporus–Neophema–Neopsephotus clade advocate recognition as a subfamily or tribe the nomenclatural details of which we will discuss elsewhere. Parenthetically, we note that crepuscular or nocturnal activity characterizes a number of species in this clade (Higgins, 1999; Forshaw, 2002) and suggest that this trait arose early in the clade’s history. Our results underscore and refine knowledge of the phylogenetic and ecological diversity of parrots in the Australo-Papuan region. Five clades or elements within them (cockatoos, polyteline parrots, core platycercines, Melopsittacus, and Neophema–Neopsephotus–Pezoporus) have diversified in Australia alone. Evolution of one platycercine species, monotypic Lathamus, has involved a loss of seed-eating and concomitant origin of nectarivory and anatomical adaptations convergent on the nectarivorous lorikeets (Gartrell et al., 2000; Gartrell and Jones, 2001). Migration has arisen at least twice (Lathamus and Neophema). There have been at least three dispersals out of Australo-Papua itself: at least one by the lories and lorikeets to the south-west Pacific islands, one by the Agapornis–Bolbopsittacus–Loriculus lineage (Schweizer et al., 2010), and the other by core platycercines (Cyanoramphus–Eunymphicus–Prosopeia; discussed above). The position of Psittacella as sister to taxa in Clades 1 + 2 + 3, regardless of some uncertainty about relationships of non-Australian genera, is at least consistent with Schodde’s ((2006); references therein) thesis of montane New Guinean being a refugium for early lineages that may have been ancestral to more xeric Australian biota (see Jønsson et al., 2011). Our phylogenetic results, however, indicate more dynamism in the evolution of the present-day ecology and biogeography rather than a simple ancestor–descendant pattern between New Guinea and Australia, respectively. Gardner et al. (2010) recently described the history of another major radiation of Australian birds, that of the passerine superfamily Meliphagoidea. They alluded to the likelihood of extinction and complex patterns of relationships between Australia and New Guinea as having been important in the evolution of the present Meliphagoidea. Our findings indicate similarly dynamic histories for parrots in the region. 4.5. Final remarks Some final systematic implications of our study concern Mayr’s (2010) tentative conclusion that the hypotarsal morphology was of limited utility in parrot systematics. He stressed that resolution of its significance depended on the position of Neophema, Neopsephotus and Micropsitta. Our study, though designed to assess the position of Psittacella and Pezoporus, shows that Micropsitta is not closely aligned with the other taxa that Mayr (2008) earlier grouped in the Loricoloriinae (Agapornis, Loriculus, lorikeets and fig-parrots and Melopsittacus). We conclude that Loricoloriinae as Mayr (2008) construed it is paraphyletic. Exclusion of Micropsitta, however, which does not appear at all close to the other relevant taxa in our analyses, still would not render Loricoloriinae monophyletic because of lingering uncertainty surrounding positions of Agapornis and Loriculus. de Kloet and de Kloet (2005) grouped Agapornis and Loriculus as sister taxa to what we have termed Clade 3 but this had relatively weak support and was based on one gene. What does seem abundantly clear from the present study and all recent phylogenetic analyses of parrots whether on anatomical or molecular data (e.g., Wright et al., 2008; Schweizer et al., 2010; Mayr, 2008, 2010) is that nomenclatural recognition is warranted for Clade 3, the lorikeet, fig-parrot-budgerigar assemblage. We will discuss details of this elsewhere. Acknowledgments AT was supported by the Australian National Wildlife Collection Foundation. Funding was provided by National Institutes of Health

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grant S06 GM008136 to TFW. The following people kindly supplied critical tissue samples or assisted in data collection: A. Nyari, A.T. Peterson, M. Robbins (Kansas University Natural History Museum, Lawrence), J. Sumner and V. Thompson (Museum Victoria, Melbourne), S, van Dyck and H. Janetzki (Queensland Museum, Brisbane), S. Murphy (Australian Wildlife Conservancy) and A. Burbidge (Western Australian Department of Environment and Conservation), G. Graves (Smithsonian National Museum of Natural History, Washington DC), P. Houde (New Mexico State University’s Vertebrate Museum, Las Cruces), D. Waugh, S. Capelli, H. Müller, J. Scharpegge (Loro Parque Funcación, Gran Canaria), T. Matsumoto, C. Miyaki (Universidad de São Paulo, São Paulo), J. Sanchez, A. Hernandez (National Institute of Toxicology and Forensic Science, Spain), and G. Chambers (Victoria University, Wellington). A. Burbidge, J. Forshaw, B. Halliday, and S. Murphy helped with discussions and laboratory aspects. S. Debus helped by stressing John Courtney’s discussions of the affinities of Pe. occidentalis. We thank Angela Frost for her expert help in preparing the figures. K. Aplin, J. Oakeshott and J. Peters commented very helpfully on drafts. Part of this work was carried out by using the resources of the Computational Biology Service Unit from Cornell University which is partially funded by Microsoft Corporation. Images of parrots from Forshaw (2006) were painted by Frank Knight and we thank author, illustrator and publisher (R. Kirk, S. Wolf, Princeton University Press) for permission to use them. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.ympev.2011.03.017. References Avise, J.C., Walker, D., 1998. Pleistocene phylogeographic effects on avian populations and the speciation process. Proc. Roy. Soc. Lond. B 265, 457–463. doi:10.1098/rspb.1998.0317. Boles, W.E., 2002. The fossil history of parrots. In: Forshaw, J. (Ed.), Australian Parrots, Robina Press, Queensland, pp. 36-40. Boon, W., Robinet, O., Rawlence, N., Bretagnolle, V., Norman, J.A., Christidis, L., Chambers, G., 2008. Morphological, behavioural and genetic differentiation within the horned parakeet (Eunymphicus cornutus) and its affinities to Cyanoramphus and Prosopeia. Emu 108, 251–260. Brereton, J.L., 1963. Evolution within the Psittaciformes. Proc. Int. Ornithol. Congr. 13, 499–517. Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T.J., Higgins, D.G., Thompson, J.D., 2003. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31, 3497–3500. Christidis, L., Schodde, R., Shaw, D., Maynes, S., 1991. Relationships among the Australo-Papuan parrots, lorikeets and cockatoos (Aves: Psittaciformes): protein evidence. Condor 93, 302–317. Condon, H.T., 1941. The Australian broad-tailed parrots. Rec. South Aust. Mus. 7, 117–144. Courtney, J., 1997. The juvenile food-begging calls and associated aspects in the ‘‘broad-tailed’’ (platycercine) parrots. Aust. Bird Watcher 17, 169–184. de Kloet, R., de Kloet, S., 2005. The evolution of the spindlin gene in birds: sequence analysis of an intron of the spindlin W and Z gene reveals four major divisions of the Psittaciformes. Mol. Phylogenet. Evol. 36, 706–721. Drummond, A., Rambaut, A., 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214. doi:10.1186/1471-2148-7-214. Eberhard, J.R., Bermingham, E., 2005. Phylogeny and comparative biogeography of Pionopsitta parrots and Pteroglossus toucans. Mol. Phylogenet. Evol. 36, 288– 304. Edwards, S.V., 2008. Is a new and general theory of molecular systematics emerging? Evolution 63, 1–19. Forshaw, J., 1969. Australian Parrots. Landsdowne Press, Melbourne. Forshaw, J., 1989. Parrots of The World. third ed. Illustrated by W.T. Cooper, Landsdowne Press, Melbourne. Forshaw, J., 2002. Australian Parrots. third ed. Illustrated by W.T. Cooper, Robina Press, Queensland. Forshaw, J., 2006. Parrots of the World. An Identification Guide. Illustrated by F. Knight. Princeton University Press, Princeton. Gardner, J., Trueman, J., Ebert, D., Joseph, L., Magrath, R.D., 2010. Phylogeny and evolution of the Meliphagoidea, the largest radiation of Australasian songbirds. Mol. Phylogenet. Evol. 55, 1087–1102. doi:10.1016/j.ympev.2010.02.00. Gartrell, B.D., Jones, S.M., 2001. Eucalyptus pollen grain emptying by two Australian nectarivorous psittacines. J. Avian Biol. 32, 224–230.

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