Phylogeny and biogeography of the fruit doves (Aves: Columbidae)

Accepted Manuscript

Phylogeny and biogeography of the fruit doves (Aves: Columbidae)

Alice Cibois, Jean-Claude Thibault, Céline Bonillo, Christopher E. Filardi, Dick

Watling, Eric Pasquet

PII: S1055-7903(13)00341-2

DOI: http://dx.doi.org/10.1016/j.ympev.2013.08.019

Reference: YMPEV 4700

To appear in: Molecular Phylogenetics and Evolution

Received Date: 17 April 2013

Revised Date: 21 August 2013

Accepted Date: 26 August 2013

Please cite this article as: Cibois, A., Thibault, J-C., Bonillo, C., Filardi, C.E., Watling, D., Pasquet, E., Phylogeny

and biogeography of the fruit doves (Aves: Columbidae), Molecular Phylogenetics and Evolution (2013), doi: http://

dx.doi.org/10.1016/j.ympev.2013.08.019

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Phylogeny and biogeography of the fruit doves (Aves: Columbidae) 1

2

Alice Cibois a*, Jean-Claude Thibaultb, Céline Bonillob, Christopher E. Filardic, Dick 3

Watlingd, Eric Pasquetb 4

5

aNatural History Museum of Geneva, Department of Mammalogy and Ornithology, CP 6434, CH 6

1211 Geneva 6, Switzerland 7

bMuséum National d’Histoire Naturelle, Département Systématique et Evolution, UMR7205 Origine, 8

Structure et Evolution de la Biodiversité, 55 rue Buffon, and Service de Systématique Moléculaire, 9

UMS2700-CNRS, 43 rue Cuvier, F-75005 Paris, France 10

cCenter for Biodiversity and Conservation, American Museum of Natural History, New York, NY 11

100024, USA 12

d Environment Consultants Fiji, Box 2041, Government Buildings, Suva, Fiji 13

*Corresponding author. Email: [email protected]; Phone: 00 41 22 418 63 02 14

15

Abstract 16

We reconstruct the phylogeny of fruit doves (genus Ptilinopus) and allies with a dense 17

sampling that includes almost all species, based on mitochondrial and nuclear sequence data. 18

We evaluate the most likely biogeographic scenario for the evolution of this group that 19

colonized many islands of the Pacific Ocean. We also investigate the evolution of one of the 20

main plumage character of fruit doves (the color of the crown), and we propose several 21

revisions of the group’s systematics. All Ptilinopus taxa formed a monophyletic group that 22

includes two morphologically distinct genera, Alectroenas and Drepanoptila, confirming a 23

previous result found with less species and genes. The divergence time analysis suggests that 1

the basal divergences within Ptilinopus dated to the Early Oligocene, and the biogeographic 2

analysis indicates that fruit doves originated most probably from the proto New Guinea 3

region. The earliest dispersals from the New Guinea region to Oceania occurred with the 4

colonization of New Caledonia and Fiji. A large group of Polynesian species (Central and 5

Eastern), as well as the three taxa found in Micronesia and four species from the Guinean-6

Mollucan region, form the “purpuratus” clade, the largest diversification of fruit doves within 7

Oceania, which also has a New Guinean origin. However, the eastbound colonization of fruit 8

doves was not associated with a significant increase of their diversification rate. Overall, the 9

Melanesian region did not act as a cradle for fruit doves, in contrast to the New Guinea region 10

which is found as the ancestral area for several nodes within the phylogeny. 11

12

Keywords 13

Island biogeography; Molecular phylogeny; New Guinea; Pacific Ocean; Polynesia; Ptilinopus. 14

1. Introduction 1

Fruit doves of the genus Ptilinopus form a large group of 50 species that have been successful 2

in colonizing many islands of the Pacific Ocean (henceforth Oceania). A significant section of 3

the genus occurs in New Guinea (24% of the taxa), whereas only a single species is found in 4

continental South East Asia, where it inhabits peninsular Malaysia. All fruit doves are 5

arboreal and frugivorous, many species playing an important role in seed dispersal of insular 6

ecosystems (Shanahan et al., 2001a; Shanahan et al., 2001b; Steadman, 1997; Steadman and 7

Freifeld, 1999). Within Oceania, the distribution of fruit doves is wide but irregular, with 8

many gaps in Micronesia, the Line Islands and from the whole Hawaiian Archipelago (Gibbs 9

et al., 2001). Although a few extinct taxa are known from remote Oceania (Kirch et al., 2010; 10

Steadman, 2006), fruit doves still occur in many remote archipelagos, on small atolls as well 11

as on larger islands such as in Fiji (Baker, 1951; Pratt et al., 1987; Watling, 2003). Molecular 12

studies of pigeons have already suggested that the fruit dove radiation includes two other 13

groups of insular pigeons, the monotypic Drepanoptila from New Caledonia, and the blue 14

pigeon genus Alectroenas from the Indian Ocean. Together with the imperial pigeons Ducula 15

and several Australasian genera (Hemiphaga, Lopholaimus, Gymnophaps), they form a large 16

clade within the Columbidae (Gibb and Penny, 2010; Pereira et al., 2007; Shapiro et al., 17

2002). Green dominates the plumage color of most fruit doves but a large variety of colors 18

and patterns exists in the group. The first phylogenetic hypotheses for Ptilinopus were based 19

on plumage similarities and size, although several species were found difficult to assign 20

because of their unique plumage pattern (Cain, 1954; Cain, 1955; Goodwin, 1967). More 21

recently, Gibb and Penny (2010) proposed a molecular phylogeny of fruit doves and imperial 22

pigeons based on a limited number of species. The results clearly demonstrated the need for a 23

comprehensive phylogeny of the fruit doves to enable a full understanding of the evolution of 24

the group. In this study we use mitochondrial and nuclear DNA sequences to address three 25

main questions on fruit doves. First, we evaluate the phylogenetic relationships among fruit 1

doves and allies with a dense sampling that includes almost all species, in order to resolve the 2

issue of the monophyly of Ptilinopus. Second, we investigate the biogeographic and temporal 3

reconstruction of the fruit doves diversification and present hypotheses for the main 4

colonization patterns that led to their diversification within Australasia and Oceania. Finally, 5

we focus on the remote Pacific colonizations, particularly in Eastern Polynesia where the fruit 6

doves are a key element of a depauperate avifauna. Additionally, we evaluate the evolution of 7

a morphological character, the color of the crown, an important character used in previous 8

phylogenetic hypotheses of fruit doves. As a result, we propose several revisions of the 9

group’s systematics. 10

11

2. Materials and methods 12

13

2.1. Taxa sampling 14

15

We sampled 44 species out of the 50 species recognized by Dickinson and Remsen (2013), 16

with at least two individuals per species for most of them. 18 species were sequenced using 17

only museum specimens as source of DNA, whereas 26 species were sequenced from fresh 18

tissue materials, with a few subspecies available only from museum specimens (see Table S1 19

for details on specimens and institutions). We were particularly interested in the fruit doves 20

endemic to the East Polynesian region (8 taxa) for which we sequenced all subspecies except 21

Ptilinopus mercierii mercierii. This taxon, now extinct, was endemic to a single island in the 22

Marquesas, and is known only by the holotype (Voisin et al., 2004) from which we were 23

unable to extract DNA successfully. The six species not included in this study represent rare 24

and localized taxa for which DNA extraction was unsuccessful using museum specimens (P. 25

dohertyi, P. subgularis, P. granulifrons, P. insolitus, and P. fischeri) or for which no tissue 1

sample was available (P. arcanus). On the basis of previously published phylogenies of the 2

Columbidae (Gibb and Penny, 2010; Pereira et al., 2007; Shapiro et al., 2002), we studied 3

also two genera that are closely related to Ptilinopus, namely Drepanoptila and Alectroenas. 4

We chose three genera for outgroups in our phylogeny: the genus Ducula, which is sister to 5

the clade composed of Ptilinopus and several related genera (see introduction), and three 6

more distantly related pigeons, the Nicobar Pigeon Caloenas nicobarica and two 7

representative of the genus Treron, the Pink-necked Green-pigeon Treron vernans and 8

Bruce's Green-Pigeon Treron waalia. 9

10

11

2.2. DNA extraction, amplification and sequencing 12

13

A standard extraction protocol was followed for the fresh tissue in the MNHN (Paris) 14

laboratory, using a commercial kit (DNeasy Tissue Kit; Qiagen, Valencia, CA, USA). The 15

museum samples were extracted in the MHNG (Geneva), using reagents exposed to UV light 16

prior to use, in a laboratory area cleaned with a 10% bleach solution prior to initiating 17

extraction. The toe pads were washed with sterile water before extraction, and the same 18

extraction protocols were followed except that the time of proteinase digestion was increased 19

from two to 12 hours, with an additional volume (20 µl) of proteinase K. Extraction tubes 20

containing no sample were used as a control for contamination. 21

We amplified portions of five genes: three mitochondrial genes, NADH dehydrogenase 22

subunit 2 (ND2) using primers L5219Met 5’-CCC ATA CCC CGA AAA TGA TG-3’ (Fuchs 23

et al., 2005), H6313 5‘-CTC TTA TTT AAG GCT TTG AAG GC-3‘ (Johnson and Sorenson, 24

1998), cytochrome c oxidase subunit I (COI) using BirdF1 (5’-TTC TCC AAC CAC AAA 25

GAC ATT GGC AC-3’) and BirdR1 (5’-ACG TGG GAG ATA ATT CCA AAT CCT G-3’) 1

(Johnsen et al., 2010) , and NADH subunit 3 (ND3) with flanking tRNAs (glycine and 2

argenine using primers L10753 (5’-GAC TTC CAA TCT TTA AAA TCT GG-3’) and 3

H11151 (5’-GAT TTG TTG AGC CGA AAT CAA C-3’) (Bowie et al., 2004); and two 4

nuclear genes, Beta-fibrinogen (FGB), exons 5 to 6 and intron 5, using primers FIB5L (5’- 5

CGC CAT ACA GAG TAT ACT GTG ACA T-3’) and FIB6H (5’- GCC ATC CTG GCG 6

ATT CTG AA-3’) (Marini and Shannon, 2002) and two new internal primers FIB-P4H (5’-7

GCA GAA CTT GAA GGA CTG CC-3’ ) FIB-P3L (5’-GGG CCT GGC TCA TTT CTT 8

AC-3’), and RAG-1 (RAG) using the primers R17L (5’-CCC TCC TGC TGG TAT CCT 9

TGC TT-3’) and R22H (5’-GAA TGT TCT CAG GAT GCC TCC CAT-3’) for most taxa, 10

and the internal primers R20H (5’-CCA TCT ATA ATT CCC ACT TCT GT-3’) R19L (5’-11

GTC ACT GGG AGG CAG ATC TTC CA-3’) for a few individuals (all RAG primers from 12

Barker et al. (2002)). 13

DNA extracted from museum specimens was degraded, so fragment sizes for 14

amplification were small (≤ 200 bp) and we focused only on the mitochondrial genes (mainly 15

ND2). Several specific ND2 primers were designed for Ptilinopus: PTL1 (5’-CAA CCY TRA 16

GCC TAC TCC T-3’), PTH1 (5’-ATT GCG ATT GCG ATT GTC AG-3’), PTL7 (5’-TCA 17

GCA CTA CTC TTA TTC TC-3’), PTH2 (5’-GAG ATG ATG GCY ATR GTG G-3’), PTL3 18

(5’-CAA CAG CAC TAA AAT TCC C-3’), PTH3 (5’-AGG TAG AAG GTT AGT AGG 19

GTT-3’), PTL4 (5’-TAG CTT TCT CTT CCA TCT CTC-3’), PTH4b (5’-CTT TGG TTG 20

CGT TGA GGG-3’), PTL5 (5’-TCA AYR CAA CCA AAG TAT TA-3’), PTH5 (5’-GTA 21

GTA TGY RAG GCG GAG GT-3’). 22

PCR amplifications were performed in 25µl reactions with 2 µl of template and 0.4 23

µM final concentration for primers. The thermocycling procedure started with an initial 24

denaturation of 3 minutes at 95°C, followed by 40 cycles of 30 seconds at 95°C, 40 seconds at 25

annealing temperature (46-55°C), and 40 seconds at 72°C for elongation. For museum 1

specimens, PCR products were purified using a purification kit (Roche Diagnostics GmbH, 2

Mannheim, Germany) and were cycle sequenced in both directions at a contract sequencing 3

facility (Macrogen, Seoul, South Korea) on an ABI3730 XL automatic DNA sequencer, using 4

the same primers as used in PCR. Contiguous sequences derived from the set of sequence 5

fragments were created using SEQUENCHER (Genecodes, Ann Arbor, MI, USA). We 6

carefully examined the sequences obtained from toe-pad extractions: because amplifications 7

could only be made for short fragments, the risks of obtaining pseudogenes or chimera are 8

higher than when using fresh material (Moyle et al., 2013). To minimize these risks, we used 9

specific primers designed to produce overlapping fragments, verified the absence of 10

amplification in the negative controls, and independently sequenced two individuals from the 11

same taxon, if possible using different sets of primers. The two individuals were also 12

extracted in different batches. We translated the nucleotide sequences to proteins using MEGA 13

5.05 (Tamura et al., 2011) and verified the absence of stop-codons or deletion in the 14

mitochondrial genes (Allende et al., 2001). 15

16

17

2.3. Phylogenetic analyses and divergence 18

The data were subjected to Bayesian inference (BI) using MRBAYES 3.2.1 (Ronquist and 19

Huelsenbeck, 2003), with models selected using MRMODELTEST 2.3 (Nylander, 2004). We 20

conducted two independent runs of 10 million generations, each with four Markov chains. 21

Markov chains were sampled every 1000 generations, with a minimum of 10% burn-in 22

period. We partitioned the data by genes (5 partitions) or by genes and codon positions (13 23

partitions), with the parameters prior unlinked and the rate prior set to variable to allow 24

variation among partitions. Results for the two partitioning schemes were evaluated with 25

Bayes factors (Brandley et al., 2005; Kass and Raftery, 1995), computed using the harmonic 1

mean from the sump command in MRBAYES. We used TRACER 1.4.1 (Rambaut and 2

Drummond, 2007) to check that we reached convergence for the posterior distributions of the 3

parameter estimates and to evaluate if a 10% burn-in was sufficient or needed to be increased. 4

We also performed phylogenetic analyses under the maximum-likelihood (ML) criterion 5

using RAXML 7.0.3 (Stamatakis, 2006), with the same partitions (partitioned by genes or 6

codon positions) and 1000 bootstrap iterations. We compared resulting topologies and nodal 7

support for all generated trees; nodes were treated as supported if posterior probabilities were 8

≥ 0.95 and bootstrap values were ≥ 70 %. Using MRBAYES, we explicitly tested the support 9

for the monophyly of the Eastern Polynesian fruit doves using a constrained analysis, and 10

evaluated the difference in harmonic mean of the likelihood of the constrained tree vs. that 11

obtained with the unconstrained topology using the Bayes factor (BF) (Kass and Raftery, 12

1995) as implemented via the sump command in MRBAYES (Brandley et al., 2005). 13

The pre-Quaternary fossil record of Columbidae is globally poor (Mayr, 2009). 14

Worthy et al. (2009) describe a columbid fossil from New Zealand, Rupephaps taketake, 15

found in a formation dated from 16 to 19 mya. This taxon shared the two morphological 16

synapomorphies that support the monophyly of the Ptilinopinae, a clade composed of the 17

genera Ptilinopus, Drepanoptila, Ducula, Lopholaimus, Gymnophas, and Hemiphaga, 18

supported also by molecular characters (Gibb and Penny, 2010; Pereira et al., 2007; Shapiro 19

et al., 2002). The fossil taxon Rupephaps was described as closely related to the extant genera 20

Lopholaimus and Hemiphaga, and its age (16-19 Ma) is congruent with the molecular 21

divergence time found in Pereira et al. (2007) for the two extant taxa: 19.2-29.6 Ma (node 36 22

in table 3). This result suggests that the divergence times obtained in Pereira et al. (2007) 23

could be used as a reasonable proxy for the basal diversification of Ptilinopines. We used 24

BEAST 1.7.4 (Drummond and Rambaut, 2007) to estimate divergence times within Ptilinopus, 25

using a relaxed-clock and the split between Ducula and the clade including Ptilinopus 1

obtained by Pereira et al. (2007), 41 Ma with 34.1-48.7 of 95% credible interval, as a basal 2

calibration point. Because it is recommended to have calibration points both at the base and at 3

the distal part of the phylogenetic tree, we used the age of an archipelago of volcanic origin, 4

the Marquesas in Eastern Polynesia, as a second calibration point. We used the age of the 5

oldest islands c.a. 5 Ma (Eiao 5.8 Ma, Nuku Hiva 4.8-3.1 Ma; Brousse et al., 1990; Legendre 6

et al., 2006) to calibrate the split leading to the Marquesas fruit doves clade. The sampling 7

was reduced to a single sequence per taxon (55 taxa in total, including outgroups) and we 8

used the models chosen for the MRBAYES analysis for the partitions by genes. We selected a 9

Yule speciation process for the tree prior and a normal distribution for the two calibration 10

points to reflect the non-directional uncertainty on the estimate (Ho, 2007). The MCMC chain 11

length was 20 million generations with a 10% burn-in period, and the same run was 12

performed several times to ensure that convergence of the models has occurred. We converted 13

the ultrametric tree obtained using BEAST to a lineage through time (LTT) plots in order to 14

visualize the temporal distribution of speciation events, using the R packages LASER 15

(Rabosky, 2007) and APE (Paradis et al., 2004). Lineage accumulation was tested for 16

departure from a constant rate hypothesis (CR) by calculating the gamma statistic (Pybus and 17

Harvey, 2000). We ran most phylogenetic analyses on the web platform Bioportal (Kumar et 18

al., 2009). 19

20

21

2.4. Biogeographic analysis 22

23

The biogeographical analysis was conducted under the DEC (dispersal extinction 24

cladogenesis) model implemented in LAGRANGE (Ree and Smith, 2008), in which the range 25

evolution along phylogenetic branches is specified by a matrix of instantaneous transition 1

rates for dispersal (equivalent to expansion) or local extinction. This matrix is used to 2

estimate the likelihoods of ancestral states along the nodes of the tree. We conducted the 3

analysis on the ultrametric tree obtained in BEAST. Eight areas of endemism were defined 4

based on the current distribution of the species studied: A Asia (treated here as the continental 5

masses West of Wallace’s line, including the Philippine Islands); B Wallacea (the group of 6

Indonesian islands between the Asian and Australian shelves); C New Guinea (including its 7

satellites islands, like Arue); D Australia; E Melanesia (from the Bismarck Archipelago to 8

Vanuatu and New Caledonia); F Central Polynesia (the region including Fiji, Tonga and 9

Samoa); G Eastern Polynesia (from the Cook Islands to the Marquesas and the Pitcairn 10

Group); H Micronesia (Marianas, Palau, and the Caroline Islands). We first conducted the 11

analysis without constraints; then an adjacency matrix was imposed in order to discard the 12

most unrealistic expansion scenarios (for instance from Asia or Wallacea directly to Eastern 13

Polynesia; Table S2). We did not impose additional expansion or time constraints. 14

15

16

2.5 Plumage evolution 17

18

The plumage of Ptilinopus is very diverse: green dominates the plumage of most fruit doves 19

but a large variety of colors and patterns exist in the group. Defining homologous plumage 20

patterns for a comparative analysis of fruit dove plumage was difficult: it seems only possible 21

within groups of closely related species, like the breast band of P. rivoli and P. solomonensis, 22

while others present a unique combination of color and patterns (like P. superbus or P. 23

aurantiifrons). We then selected a single, well-defined character, the crown color, which was 24

used for instance by morphologists to define one of the main “natural groups” (meaning 25

monophyletic), the “purpuratus” clade (Cain, 1954; Goodwin, 1967; Ripley and Birckhead, 1

1942). A colored crown is a widespread feature in Ptilinopus, sometimes associated with 2

sexual dimorphism. We coded this character for all fruit doves (males only) using five states: 3

(0) no distinct colored crown, (1) red crown (including purple, pink, crimson etc.), (2) blue 4

crown, (3) grey crown, and (4) white crown. We inferred ancestral state reconstruction at each 5

node within the fruit dove phylogenetic tree using a maximum likelihood approach 6

implemented in MESQUITE 2.74 (Maddison and Maddison, 2010) with the Mk1 rate model 7

(Lewis, 2001). 8

9

10

3. Results 11

12

3.1 Phylogenetics 13

14

The final data set included 134 individuals representing 55 taxa, with 47 Ptilinopus, 2 related 15

genera (Drepanoptila and Alectroenas) and 6 outgroups. Within Ptilinopus, 41 individuals 16

(19 taxa) were represented by toe-pad samples from museum specimens. We sampled several 17

individuals per taxon (two for museum specimens) except for a few taxa (P. purpuratus 18

chrysogaster, P. perlatus, P. insularis, P. eugeniae, P. chalcurus, P. aurantiifrons). We 19

included one sequence from GenBank (P. rivoli; accession number GU230717; Gibb and 20

Penny, 2010). We obtained sequences for ND2 (1041 bp), ND3 (352 bp, and 396 bp when 21

including partial flanking tRNA), COI (694 bp), RAG1 (1076 bp), and FBG (579 bp). For the 22

taxa extracted from museum specimens, we focused only on the mitochondrial genes (mainly 23

ND2, with shorter sequences for a few individuals). New sequences were deposited in 24

GenBank under accession numbers KF446677-KF447112 (Table S1). The alignments were 25

straightforward, with no indels for the RAG1, COI and ND2 sequences and four indels in 1

FBG. The ND3 sequences presented one extra nucleotide non translated in position 174, a 2

situation found in several species of birds (Mindell et al., 1998). Results from the Akaike 3

information criterion (AIC) values in MODELTEST for the 13 partitions are indicated in Table 4

S3. Estimated likelihood harmonic means were -22638.18 for the partition by gene and -5

21631.76 for the partition by codon position. Differences in Bayes factors were significant for 6

the most complex model. 7

All Ptilinopus taxa formed a monophyletic group (Figs 2A and B) that includes two 8

morphologically distinct genera, Alectroenas and Drepanoptila, confirming a previous result 9

found with less species and genes (Gibb and Penny, 2010; Shapiro et al., 2002). Within 10

Ptilinopus, the first clade to branch off was composed of two large species, P. magnificus and 11

P. bernsteinii, sometimes placed in their own subgenus Megaloprepia (see discussion). The 12

next clade included all the species from the Philippines (P. occipitalis, P. leclancheri, P. 13

marchei, and P. merrilli) and, embedded within them, the only Ptilinopus that inhabits 14

continental South East Asia (P. jambu). The Philippines species have been placed by some 15

authors in the subgenus Ramphiculus (see discussion). Whereas these basal nodes of the 16

phylogeny are all well-supported, the position of the following taxa were uncertain in all 17

analyses, with very short branches: the Blue Pigeon Alectroenas from the Indian Ocean, the 18

Cloven-feathered Dove Drepanoptila holosericea from New Caledonia, the small P. nainus 19

from New Guinea, the clade formed by three species endemic to Fiji [P. victor, P. luteovirens, 20

and P. layardi) sometimes placed in their own genus Chrysoena (Wolters 1975-1982; see 21

remarks in the acknowledgments for the spelling of this genus)], another Asian species (P. 22

melanospilus), and the two sister taxa from the Sunda and lesser Sunda islands (P. porphyreus 23

and P. cinctus). The next supported clades were formed by Moluccan and Melanesian species: 24

first a group of three species (P. superbus, P. rivoli, and P. solomonensis), second a larger 25

group of nine species with some irresolution between them (P. eugeniae/P. viridis, P. iozonus, 1

P. perlatus/P. wallacii/P. aurantiifrons/P. ornatus, P. hyogastrus, P. tannensis). The 2

remaining species formed a clade often recognized as the “purpuratus” group by 3

morphologists, mainly based on the presence of a distinct crown and of bifurcated breast 4

feathers (Cain, 1954; Goodwin, 1967; Ripley and Birckhead, 1942). At the base of this group, 5

the position of two small species from the Moluccan and New Guinea regions was not well 6

supported in the Bayesian analysis (support >70% in ML): P. pulchellus and P. monacha (the 7

later with the only blue crown known in Ptilinopus). Similarly, the relative position of the 8

Moluccan P. regina and the New Guinean P. coronulatus was uncertain in both analyses. All 9

fruit doves from Eastern Polynesia belonged to the same clade that comprised also species 10

from Micronesia, Melanesia and Central Polynesia. The first to branch off within this large 11

Pacific clade were the two species endemic to the Marquesas Islands (P. dupetithouarsii and 12

P. mercierii). The remaining phylogenetic relationships were not well supported except for 13

the three following clades: 1) the clade including P. porphyraceus and P. greyi, 2) the group 14

formed by the Palau endemic P. pelewensis, the Melanesian P. richardsii and the fruit dove 15

endemic to the Marianas P. roseicapilla, and 3) the clade formed by all remaining Eastern 16

Polynesian taxa. The Many-colored Fruit Dove P. perousii, from Central Polynesia, was 17

found in all analyses to be sister taxon to the Eastern Polynesian clade but with weak support. 18

The Eastern Polynesian clade was divided in two well-supported groups: first, the species 19

endemic to the southern part of this region (P. coralensis and P. chalcurus from the Tuamotu, 20

P. huttoni from Rapa, P. insularis from Henderson); second the species found in the Cook (P. 21

rarotongensis) and Society Islands (P. purpuratus purpuratus, P. purpuratus frater, P. 22

purpuratus chrysogaster). P. purpuratus was found not to be monophyletic, with the taxon 23

chrysogaster found to be a sister taxon to P. rarotongensis with good support. There were 24

significant differences when using Bayes factors between the best tree (Figs 2A and B) and 25

the tree constrained for the monophyly of the Eastern Polynesian taxa (i.e. the strict clade 1

formed by the eastern Polynesian clade plus the Marquesas clade). The harmonic mean of the 2

log likelihood of the unconstrained analysis was -21631.76. When we constrained the 3

monophyly of the Eastern Polynesian fruit doves, the harmonic mean was -21697.89 and 4

2LnBF = 132.26, a value superior to 10 providing strong evidence against the constrained 5

trees (Kass and Raftery, 1995). This result favored the rejection of a clade formed solely by 6

Eastern Polynesian fruit doves, and the recognition of a clade covering a large part of the fruit 7

doves range in the Pacific, including the most remote islands. 8

9

10

3.2. Divergence time and biogeography 11

12

The divergence time analysis, summarized as a chronogram in Fig. 3, suggests that the basal 13

divergences within Ptilinopus dated to the Early Oligocene (≈ 33 - 30 Ma). We obtained very 14

similar results for the biogeographical analyses with or without an adjacency matrix, with a 15

similar global likelihood (2∆ln= 4.4, not significant; Kass and Raftery, 1995) and better 16

relative likelihoods at the nodes for the analysis with an adjacency matrix (results shown in 17

Fig. 4). The most likely ancestral areas for the basal nodes of the phylogenetic tree are the 18

New Guinea region (the “proto New Guinea”, emerging at this time from the Australian-19

Papuan plate; Hall, 2002), and the Asian plate. Several short branches, representing the split 20

of multiple lineages over a short period of time, occurred during the Early Miocene (≈ 20 21

Ma). Most of these lineages originated from the “proto New Guinea” area. During the 22

Miocene (≈ 16-6 Ma), the fruit doves continued to diversify within the New Guinea region, 23

and several lineages dispersed also from the New Guinea to the adjacent Melanesia and 24

Moluccas. The dispersal to remote Oceania occurred probably between 8 to 6 Ma, more likely 25

from the New Guinea region. This long distance dispersal was followed rapidly by the 1

colonization of one of the Eastern Polynesian archipelago, the Marquesas, at the beginning of 2

the Pliocene (≈ 5 Ma). During the Pliocene, diversification occurred within Central Polynesia 3

and Micronesia, with two independent dispersals from Micronesia to Melanesia around the 4

Pliocene/Pleistocene boundary (≈ 2.5-2 Ma). The second colonization of Eastern Polynesia 5

occurred at the end of the Pliocene (≈ 3Ma), and most of the diversification within this region 6

took place during the early Pleistocene (≈ 2Ma). 7

Lineage-through-time (LTT) plots (Fig. 3) showed the temporal accumulation of 8

lineages for the entire ingroup: some fluctuation occurred but the hypothesis of a constant rate 9

model was not rejected (g = -0.247, P = 0.40). 10

11

12

3.3 Plumage evolution: the crown coloration 13

14

The analysis using MESQUITE (Fig. 5) showed that the absence of a distinctive crown color is 15

a pleisiomorphic characters among fruit doves, shared by the oldest linages within the 16

phylogenetic tree. It also suggested that colored crowns appeared four times, always with a 17

red pigmentation: basal to the P. rivoli/P. solomonensis/P. superbus group, twice 18

independently within the P. wallacii clade (P. aurantiifrons and P. wallaceii), and basal to the 19

“purpuratus” group. Within this clade, the crown coloration evolved three times from the red 20

coloration to an autopomorphic color: blue for P. monacha, grey for P. richardsii, and white 21

for P. dupetithouarsii. 22

23

24

4. Discussion 25

1

4. 1 Biogeography: the role of New Guinea 2

3

At the time of the origin of the fruit dove radiation, what corresponded to the present-day 4

New Guinea was formed by the northern rim of the Australo-Papuan plate, which began to 5

emerge at the Eocene-Oligocene boundary as a result of the collision with the Asian plate 6

(Hall, 1998; Hall, 2002). The biogeographic analysis based on the DEC model in LAGRANGE 7

suggested that fruit doves originated from this proto New Guinea region (Fig. 4). Previous 8

studies have already enlightened the importance of this region in the diversification of another 9

large group of land birds, the songbirds (Passeriformes) (Barker et al., 2002; Ericson et al., 10

2002). Within a temporal frame similar to the fruit dove radiation, the early radiation of the 11

core Corvoidea (including the Campephagidae, cuckoo-shrikes) coincided with the emergence 12

of the proto New Guinea at the boundary of the Eocene and Oligocene (Jønsson et al., 2011). 13

The basal splits within Campephagidae suggested an early dispersal from the Australo-14

Papuan region to Asia during the Oligocene, when the distance between the two plates was 15

decreasing (Fuchs et al., 2007; Jønsson et al., 2008). Similarly, the fruit doves rapidly 16

expanded their range to the Asian plate during this period (Figs 3 and 4). Fruit doves have 17

been very successful in colonizing several remote archipelagoes in Oceania, flying over vast 18

distances of sea (hundreds of kilometers in the case of Eastern Polynesia, see below). 19

Nevertheless, it is likely that the reduction of distances between the Australo-Papuan region 20

and Asia during the Oligocene favored their dispersal like cuckoo-shrikes. 21

Within the Asian fruit dove clade, P. marchei and P. merrilli are restricted to the 22

northern part of the actual Philippines (mainly Luzon Island), a region that was connected by 23

shallow sea to the Asian plate at the Early Miocene, whereas the eastern Philippines had 24

another origin (the Philippines Sea Plate) and rejoined the northern part of the actual 25

Philippines much later (Hall, 1998, fig. 15). Compared to the species with a larger distribution 1

within the Philippines and beyond in South East Asia (i.e. the clade formed by P. occipitalis, 2

P. leclancheri, and P. jambu), the restricted distribution of P. marchei and P. merrilli suggests 3

that they may represent offshoots of the early dispersal of fruit doves to the Asian continent. 4

The New Guinean region continued to play an important role in fruit doves’ 5

diversification with many lineages arising from this region during the Early Miocene (ca. 20 6

Ma). This period corresponded also to the dispersal of a lineage of fruit dove toward the 7

Indian Ocean, leading to the diversification of the blue pigeons Alectroenas (four species) that 8

colonized the main islands of Madagascar, Comoro, Seychelles, and Mauritius (the latter 9

extinct since the 19th century). The fact that the blue pigeons colonized the Indian Ocean 10

islands from the Australasian region confirms a direct colonization route that has been 11

hypothesized for cuckoo-shrikes (Jønsson et al., 2008) and parrots (Kundu et al., 2012; 12

Schweizer et al., 2009). 13

14

15

4. 2 Biogeography: the early colonizations of Oceania 16

17

The earliest dispersals from the New Guinea region to Oceania occurred with the colonization 18

of New Caledonia and Fiji. The LTT analysis (Fig. 3) suggested however that the eastbound 19

colonization of fruit doves was not associated with a significant increase of their 20

diversification rate. New Caledonia is an old island of Gondwana origin but with a long 21

period of submergence that ended 37 Ma (Grandcolas et al., 2008). This lineage is represented 22

by the Cloven-feathered Dove Drepanoptila holosericea, a monospecific genus, which share 23

some morphological and behavioral similarities with fruit doves (Gibbs et al., 2001) but 24

presents also apomorphic feather characters (fluffed white feathers on the tarsi, modified 25

primary tips curved forward and deeply cleft at the shaft, producing a loud whistling in 1

flight). The second dispersal from the New Guinea region to Oceania led to the colonization 2

of Fiji by the golden doves group (P. victor, P. layardi and P. luteovirens, often included in 3

their own genus Chrysoena). In both cases the topology of the tree was not well-supported, 4

with the P. melanospila/golden dove group and P. nainus/Drepanoptila sister taxa 5

relationships not recovered in the Bayesian and ML analyses with a denser sampling (Fig. 6

2A). Uncertainties remain for the dates of these dispersals, but the short branches of the tree 7

suggested that the earliest dispersals to Oceania occurred during the Early Miocene (ca. 20 8

Ma), probably from the New Guinea region. Irestedt et al. (2008) suggested that an enigmatic 9

bird endemic to Fiji, the Silktail Lamprolia victoriae, diverged from its Papuan sister species 10

at the same period of time during the Miocene. It is possible then that the geology of the 11

Melanesian Arc provided at this time partial connections between the New Guinea region and 12

the Fiji islands (Hall, 2002). 13

Diversification within the New Guinea region continued during the Miocene, and led 14

to several range expansions to both east (the Melanesian region) and west (the Mollucas): the 15

lineage leading to P. tannensis, the P. solomonensis/ P. rivoli/ P. superbus clade (the latter 16

also found in Australia), the P. viridis/ P. eugeniae clade, and two species within the 17

“wallacii” clade (P. wallacii and P. hyogastrus). P. tannensis is basal within the “wallacii” 18

clade, with a divergence time estimated at 9 Ma. Endemic to Vanuatu, it is currently found 19

throughout the archipelago. The geology of Vanuatu is complex, with four main periods of 20

volcanic activity, the oldest around 22 Ma, the youngest around 3 Ma (Gillespie and Clague, 21

2009). P. tannensis corresponds to the oldest lineage colonizing this archipelago, probably at 22

a time when several islands provided suitable habitats for fruit doves. Vanuatu was recently 23

colonized by a second fruit dove (P. greyi), this time from a Pacific origin (see next 24

paragraph): this taxon is also present in New Caledonia (but only the offshore islands) and the 25

south of the Solomon Islands (Dutson, 2011). A similar pattern is found for the Solomon Is., 1

with both old (Miocene) colonizations originating from the New Guinea region (the P. 2

solomonensis/ P. superbus group, the lineage leading to P. viridis and P. eugeniae) and two 3

recent (Pliocene-Pleistocene) dispersals within the “purpuratus” group (P. richardsii and P. 4

greyi), with a Pacific origin. It is worth noting that, according to our biogeographic analysis 5

based on the current distribution of the taxa (Fig. 4), the Melanesian region did not act as a 6

cradle for fruit doves, in contrast to the New Guinea region which is found as the ancestral 7

area for several nodes within the phylogeny. 8

9

10

4. 3 The “purpuratus” group and the evolution within Eastern Polynesia 11

12

This clade comprises 19 species, most of which composing the “purpuratus” group defined 13

by morphologists (Cain, 1954; Goodwin, 1967; Ripley and Birckhead, 1942). It was found 14

monophyletic in all analyses with good support (Fig. 2B). It includes all the remaining 15

Polynesian species (Central and Eastern), as well as the three taxa found in Micronesia and 16

four species from the Guinean-Molucan region. The sister clade of the “purpuratus” group 17

originated from New Guinea, and the two basal species within this clade, P. pulchellus and P. 18

monacha, are also endemic to this region. The most likely ancestral area for the “purpuratus” 19

clade is logically the New Guinean region (Fig. 4). Within this clade, the strict monophyly of 20

the Eastern Polynesian taxa was rejected, suggesting that this remote part of Oceania was 21

colonized twice during the diversification of the fruit doves, first the Marquesas and later the 22

remaining archipelagos (from the Cook Is. to Pitcairn Group). The intriguing situation in the 23

Marquesas, where two endemic, sympatric species, are also sister species with good support 24

in the phylogenetic analysis, is developed elsewhere (Cibois et al. unpublished). The other 25

Eastern Polynesian archipelagos were colonized ca. 2 Ma, after the formation of the oldest 1

islands of the group (4.2-4.5 Ma for Maupiti in the Society Is., 4 Ma for Rapa in the Austral 2

Is.; Dickinson, 1998; Guillou et al., 2005). 3

The analysis of plumage coloration shows that the red crown (including all variations 4

from orange to purple) is the plesiomorphic state for this character within the “purpuratus” 5

group (Fig. 5). The color is based on carotenoid pigments (Mahler et al., 2003) and three taxa 6

evolved from this red coloration to other colors which are probably based on structural 7

coloration (Gill and McGraw, 2006): blue in P. monacha, white in P. dupetithouarsii, and 8

grey in P. richardsii. Experiments have shown that in a feather of the American Goldfinch 9

(Carduelis tristis) the yellow color was actually produced by a combination of carotenoids 10

pigments with an underlying white structural coloration (Shawkey and Hill, 2005). Thus, the 11

white crown (and malar patch) of P. dupetithouarsii could result from the disappearance of 12

the carotenoid pigments that are still present in its sister and sympatric species P. mercierii. 13

However, the mechanisms of most of the structural colors are largely unknown and further 14

studies on the fruit dove coloration mechanisms will be necessary for testing the color 15

evolution of their plumage. 16

17

18

4. 4 Systematics 19

20

Molecular phylogenies (Gibb and Penny, 2010; Shapiro et al., 2002; this work) support the 21

inclusion within the fruit dove radiation of two morphologically quite distinct genera, 22

Drepanoptila Bonaparte, 1855 and Alectroenas Gray, 1840, thus making the genus Ptilinopus 23

Swainson, 1825 paraphyletic in its current definition. The classification of birds should 24

ultimately reflect their phylogenetic relationships (Cracraft et al., 2004), and taxa above the 25

species level should be defined as monophyletic groups. To achieve this goal for fruit doves, 1

one can merge all three genera into the oldest name Ptilinopus, but this large group of 55 2

species would however be fairly heterogeneous, on both morphological and biogeographic 3

basis. We suggest an alternative solution that corresponds to the use of different genera for the 4

main fruit dove lineages. 5

First, the genus Megaloprepia Reichenbach (type species Columba magnifica 6

Temminck), used by Peters (1937) and Cain (1954), and merged with Ptilinopus by Goodwin 7

(1967). It was composed of the two species P. magnificus and P. bernsteinii (for which the 8

first name Megaloprepia formosa Grey, 1860, previously preoccupied in Ptilinopus, should 9

be used again following the Article 59.4 of the International Code of Zoological 10

Nomenclature; International Commission of Zoological Nomenclature, 1999), on the basis of 11

their bright yellow under-wing coverts, a character unique among fruit doves. These two 12

species form the first basal clade within the fruit doves’ phylogenetic tree, with good support 13

in all analyses. 14

Second, the genus Ramphiculus Bonaparte (type species Ptilinopus occipitalis Gray), 15

merged with Ptilinopus by Peters (1937) and Goodwin (1967), and resurrected by Cain (1954) 16

for six species found in the Philippines and Sulawesi: P. marchei, P. merrilli, P. occipitalis, 17

P. fischeri, P. leclancheri, and P. subgularis. Cain based this group of fruit doves on their 18

medium size and on their colored pattern on the side of the head, sometime reaching the hind 19

neck (although absent in P. leclancheri). Four of them formed a well-supported clade in our 20

analysis, first with the two sister species from the Northern Philippines P. marchei and P. 21

merrilli, second with P. occipitalis from the Philippines and sister to the clade formed by P. 22

leclancheri (widespread in the Philippines and Taiwan) and P. jambu, the only fruit doves 23

found in continental South East Asia. The unique plumage pattern of P. jambu (the male 24

exhibits a bright pinkish-red face) was a puzzle for morphologists who did not agree on its 25

relationships with the other fruit doves (Cain, 1954; Goodwin, 1967). Its position within the 1

molecular phylogenetic tree suggests that this peculiar species belongs to a group of species 2

with a common biogeographic origin. The two last species not sampled in our analysis, P. 3

fischeri and P. subgularis (both from Sulawesi), may also belong to this clade on the basis of 4

their morphological features. 5

We then suggest retaining Drepanoptila, Alectroenas, and Chrysoena as genera based 6

on morphological divergence. Because the relationships between these taxa and several fruit 7

doves (P. nainus, P. melanospilus, P. porphyreus and P. cinctus) are not supported (Fig. 2A), 8

there is however a risk that, as defined, Ptilinopus may not be monophyletic: additional 9

genetic data might be necessary to resolve this part of the phylogenetic tree. 10

11

At the species level, our phylogeny shed light into several cases where the current 12

taxon definition requires further investigation. We sampled two allopatric populations of the 13

Crimson-crowned Fruit Dove P. porphyraceus, the nominate subspecies from Tonga in 14

Central Polynesia and the subspecies ponapensis from the Caroline Islands in Micronesia. 15

They did not form a monophyletic group because of the inclusion of the Red-bellied Fruit 16

Dove P. greyi (sampled in Vanuatu and Loyalty Islands and monophyletic), sister with good 17

support to ponapensis. All three taxa share similar plumage patterns and deciphering their 18

relationships will require the sampling of the remaining four subspecies of P. porphyraceus 19

that inhabit Micronesia and the Central Polynesia. The white-headed Fruit Dove P. eugeniae, 20

endemic to a group of islands in the southern part of the Solomon Islands, was found 21

embedded within individuals of the Claret-breasted Fruit Dove P. viridis, a species 22

widespread in the islands of New Guinea and the northern part of the Solomon Islands. 23

Except for the color of the head, both taxa share a very similar plumage pattern suggesting, 24

along with their allopatric distribution, a recent common ancestry that could cause the 1

paraphyly of P. viridis by incomplete lineage sorting. 2

In Eastern Polynesia, the two taxa found in the Tuamotu Archipelago, recently treated 3

as distinct species (Dickinson, 2003; Dickinson and Remsen, 2013; Pratt et al., 1987), are the 4

Atoll Fruit Dove P. coralensis, widespread in more than thirty islands, and the Makatea Fruit 5

Dove P. chalcurus endemic to the island of Makatea, an atoll uplifted in the early Pleistocene 6

as the result of lithospheric loading by the Tahiti-Moorea-Mehetia complex (Montaggioni, 7

1989). The two taxa differ only by their cap, incomplete and pinkish in coralensis, large and 8

purple in chalcurus. We found no variation between coralensis and chalcurus for the 9

mitochondrial genes COI and ND3, and a single transition between coralensis and chalculus 10

for ND2. In addition with the minor plumage difference, these results suggest that the two 11

taxa might be best treated as subspecies of P. coralensis. The result for fruit doves contrasts 12

with the one found for another land bird, the Tuamotu Reed Warbler (Acrocephalus atyphus), 13

for which the populations found on uplifted atolls (Makatea, Niau, and Anaa) can be 14

diagnosed by a combination of morphological (morphometrics) and molecular characters 15

(mitochondrial and microsatellites) (Cibois et al., 2010). Within the Marquesas, we sampled 16

the two subspecies described for P. dupetithouarsii and found no reciprocal monophyly. 17

Although our sampling was limited to a few individuals per islands, the absence of a 18

geographical structure in the genetic data suggested ongoing gene flow or incomplete lineage 19

sorting. Finally, in the Society Islands the Grey-green Fruit Dove P. purpuratus may not be 20

monophyletic, with the subspecies chrysogaster from the Leeward Islands more closely 21

related to P. rarotongensis from the Cook Islands (a rare taxon in the museum collections) 22

than with the subspecies found in Tahiti (nominate) and Moorea (frater). However, denser 23

sampling will be necessary to confirm this result. 24

25

1

Acknowledgments 2

We are grateful to the following people and institutions for providing tissue or toe-pad 3

samples: Joel Cracraft and Paul Sweet (American Museum of Natural History), Donna 4

Dittmann and Frederick Sheldon (Louisiana State University), Sharon Birks (University of 5

Washington, Burke Museum), Jon Fjeldså (Zoological Museum of Copenhagen), Clemency 6

Fisher and Tony Parker (National Museums Liverpool), Robert Prys-Jones and Mark Adams 7

(Natural History Museum, Tring), and Erica Spotswood (University of Berkeley). For their 8

help and support during fieldworks in French Polynesia and New Caledonia, we thank Jean-9

Yves Meyer (Research delegation of the Government of French Polynesia), Philippe Raust 10

and Thomas Gesthemme (Société d’Ornithologie de Polynésie), Claude Serra (Direction de 11

l’Environnement, French Polynesia), the Institut pour la Recherche et le Développement (IRD 12

Tahiti), Julien Baudat-Franceschi (Société Calédonienne d'Ornithologie), Almudena Lorenzo 13

and Mariane Bonzon (Parc Zoologique et Forestier de Nouméa), Péguy and Jean-Pierre Drain 14

(Nouméa). We thank Jérôme Fuchs (MNHN) for assistance with analyses made using R and 15

Guy Arnaudo (MNHN) for his work during the initial part of the lab. We are grateful to Les 16

Christidis, Norman David, Edward Dickinson, Steven Gregory, and Richard Schodde for their 17

research on the correct spelling of the genus Chrysoena: this issue may not be completely 18

resolved and further research will be published elsewhere. This work was supported by the 19

Consortium National de Recherche en Génomique, and the Service de Systématique 20

Moléculaire of the Muséum National d’Histoire Naturelle in Paris (CNRS UMS 2700). It is 21

part of the agreement no. 2005/67 between the Genoscope and the Muséum National 22

d’Histoire Naturelle on the project ‘Macrophylogeny of life’ directed by Guillaume Lecointre. 23

24

25

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24

Figure legends 1

2

Figure 1: Distribution of Ptilinopus fruit doves. The number indicates the number of species 3

found on each region or archipelago according to Dickinson and Remsen (2013). 4

5

Figure 2 : Phylogenetic tree of fruit doves (Ptilinopus ssp.) and allies, based on mitochondrial 6

and nuclear sequence data, estimated using Bayesian and maximum likelihood inferences. 7

Asterisks indicate nodes supported by posterior probabilities (PPs) ≥ 0.95 and bootstrap (BT) 8

values ≥ 70%. When support differs between methods, PPs are indicated first and BT second 9

with support below significance labeled by a dash. 10

11

Figure 3 : (a) Lineage-through-time plots (LTT), showing the number of extant lineages (ln) 12

for the ingroup. (b) Bayesian chronogram for the fruit doves and allies inferred using BEAST. 13

Error bars represent 95% posterior intervals. All time scales are in Ma. 14

15

Figure 4: Biogeographic analysis of fruit doves using LAGRANGE, based on the chronogram 16

obtained with BEAST (Time scale in Ma). Eight areas of endemism were defined: A Asia 17

(including the Philippine Islands); B Wallacea; C New Guinea; D Australia; E Melanesia; F 18

Central Polynesia; G Eastern Polynesia; H Micronesia (see methods for details). Results at the 19

nodes indicate the ranges inherited by each descendant branch; capitals letters indicate a 20

relative probability ≥ 70% for the node, lower cases a relative probability ≤ 70%. Stars 21

indicate dispersals to Oceania. 22

Figure 5: Ancestral state reconstructions for the crown coloration of fruit doves using 1

MESQUITE (Maximum likelihood inference). The “red” state includes all reddish color 2

variations like purple, pink, crimson etc. 3

30°

0°

30°

150°O180°150°E

Scale 1 : 35 000 000at the equator

3500 km0

Australia

Marquesas

Cook

Austral

Society

Tuamotu

Pitcairn

Fiji

Philippines

NewGuinea

Sundas

Samoa

Tonga

Solomons

Carolines

Marianas

Vanuatu

New Caledonia

PalauBismarcks

Moluccas12

8

5

5

6

5

(1 incl.SE Asia)

3

4

2

2

1

1

1

1

1

1

1

22

22

DrepanoptilaAlectroenas

P. (Ramphiculus) occipitalis

P. (Megaloprepia) magnificus

*

*

*

**

*

* *

**

*

**

*

*

*

*

*

*

**

*

*/-

*

*-/*

*

**

*

*

*

*

**

*

*

*

*

*

*-/*

-/*

**

**

*

* *

*

*

0.4

P. (Chrysoena) victor

4 Sibuyan Philippines1 Australia2 Australia

3 (captive)4 (captive)

P. magnificus

2 Moluccas P. bernsteinii

Megaloprepia

Caloenas nicobaricaTreron waalia

Treron vernans

1 Moluccas

Ducula aenaD. pacifica

D. bicolor

5 (captive)3 Sibuyan Philippines1 Mindanao Philippines2 Mindanao Philippines

P. occipitalis

1 Papua New Guinea2 Papua New Guinea P. nainus

(captive)(captive)1 Luzon Philippines2 Luzon Philippines P. marchei

P. merrilli1 Luzon Philippines2 Luzon Philippines

1 Sibuyan Philippines2 Sibuyan Philippines

P. leclancheri1 Singapore2 Singapore P. jambu Ramphiculus

Drepanoptila holosericeaAlectroenas pulcherrimus


3 (captive)P. melanospilus

1 Fiji2 Fiji P. luteovirens

1 Kandavu Fiji2 Kandavu Fiji

P. layardi1 Tavini Fiji2 Vanua Fiji P. victor

Chrysoena


1 Isabel Solomons2 Australia3 Choiseul Solomons4 Malaita Solomons5 New Georgia Solomons6 Australia

P. superbus


1 (captive)P. porphyreus

1 Sunda2 Sunda P. cinctus

1 North Moluccas2 North Moluccas P. hyogastrus

P. tannensis1 Vanuatu2 Vanuatu

1 Makira Solomons2 Makira Solomons3 Makira Solomons4 Makira Solomons5 Makira Solomons6 Makira Solomons

P. solomonensis

(captive) P. rivoli

Makira Solomons2 Choiseul Solomons3 New Georgia Solomons

1 Guadalcanal SolomonsP. viridis

P. eugeniae


P. iozonusP. perlatus(captive)

(captive) P. aurantiifrons1 Papua New Guinea2 Papua New Guinea P. ornatus

1 Babar Moluccas2 Tanimbar Moluccas P. wallacii

the "purpuratus" group

*4 Tahiti (purpuratus)9 Tahiti (purpuratus)

6 Tahiti (purpuratus)7 Tahiti (purpuratus)2 Moorea (frater)3 Moorea (frater)

P. purpuratus

P. rarotongensis

P. coralensisP. chalcurusP. insularisP. huttoni

P. perousii

P. porphyraceus

P. porphyraceus

P. greyi

P. roseicapilla

P. richardsii

P. pelewensis

P. dupetithouarsii

1 Palau2 Palau

10 Ua Pou (viridior)11 Ua Pou (viridior)

7 Nuku Hiva (viridior)4 Ua Huka (viridior)6 Ua Huka (viridior)

9 Nuku Hiva (viridior)8 Nuku Hiva (viridior)

1 Fatu Hiva (dupetithouarsii)5 Ua Huka (viridior)

2 Tahuata (dupetithouarsii)3 Tahuata (dupetithouarsii)

1 Owa Rahau Solomons2 Owa Rahau Solomons

1 Rota Marianas2 Rota Marianas

3 Pohnpei (ponapensis)2 Pohnpei (ponapensis)

1 Eua Tonga (porphyraceus)2 Eua Tonga (porphyraceus)

1 Vanuatu2 Vanuatu

3 Lifu4 Lifu

1 Eua Tonga2 Fiji

1 Rapa2 Rapa

1 Tikehau2 Manihi

1 Huahine (chrysogaster)

P. purpuratus

8 Tahiti (purpuratus)5 Tahiti (purpuratus)

1 Rarotonga (rarotongensis)2 Atiu (goodwini)

3 Atiu (goodwini)

MakateaHenderson

1 Hiva Oa (tristrami)2 Hiva Oa (tristrami)3 Hiva Oa (tristrami)

P. mercierii

4 Wulur Indonesia (xanthogaster)5 Melville Australia (regina)

1 (captive)2 (captive)3 (captive) P. regina

1 Papua New Guinea2 Papua New Guinea

P. coronulatus

1 Halmahera Moluccas2 Halmahera Moluccas

P. monacha

P. pulchellus1 Papua New Guinea2 Papua New Guinea

**

**

**

*

**

*

*

*

****/-

*/-

*

***

*

*

**

-/* **

*

*-/*

*

**

*

the "purpuratus" group

P. purpuratus

P. monacha

P. perousii

*

P. p. frater

P. rarotongensis

P. coralensisP. chalcurus

P. insularisP. huttoniP. perousii

P. porphyraceus

P. porphyraceusP. greyi

P. roseicapilla

P. richardsiiP. pelewensis

P. purpuratus

P. p. chrysogaster

P. dupetithouarsii

P. mercierii

P. reginaP. coronulatus

P. monachaP. pulchellus

P. viridis

P. eugeniae

P. iozonusP. perlatus

P. aurantiifronsP. ornatusP. wallaciiP. hyogastrus

P. tannensisP. solomonensisP. rivoliP. superbus

P. porphyreus

P. cinctus

P. melanospilus

P. luteovirensP. layardi

P. victor

P. nainusD. holosericea

A. pulcherrimus

P. marcheiP. merrilli

P. leclancheri

P. jambuP. occipitalis

P. magnificusP. bernsteinii

D. aena

D. pacifica

D. bicolor

C. nicobaricaT. waaliaT. vernans

0 5 10 15 20 25 30

1.0

1.5

2.0

2.5

3.0

3.5

4.0

Log−Lineages Through Time

Time From Basal Divergence

Log

Line

ages

o

o

o

oooo

ooooooo o oo

o ooooooooooooooooooooooooooooooo

50 40 30 20 10 0

(a) (b)

P. p. frater G

P. rarotongensis G

P. coralensis GP. chalcurus G

P. insularis GP. huttoni GP. perousii F

P. p. ponapensis H

P. porphyraceus FP. greyi E

P. roseicapilla HP. richardsii EP. pelewensis H

P. purpuratus G

P. p. chrysogaster G

P. dupetithouarsii GP. mercierii G

P. regina BDP. coronulatus C

P. monacha BP. pulchellus C

P. viridis BCEP. eugeniae E

P. iozonus CP. perlatus CP. aurantiifrons CP. ornatus CP. wallacii BCP. hyogastrus BP. tannensis EP. solomonensis CEP. rivoli BCEP. superbus BCDE

P. porphyreus AP. cinctus AB

P. melanospilus ABP. luteovirens FP. layardi FP. victor F

P. nainus CD. holosericea E

A. pulcherrimus A

P. marchei AP. merrilli A

P. leclancheri AP. jambu AP. occipitalis A

P. magnificus CDP. bernsteinii B

D. aena BD. pacifica CEFG

D. bicolor ABCD

C. nicobarica ABCT. waalia AT. vernans AB

A

B C

D

E F G

H

cc

FC

fg

cc

GG

EH

fh

fhffhh

GF

GG

HE

cc

CC

CC

cc

CCCC

CC CC

CC

CC

EBCE

cc

cc

CC

CC

CC

AA

cc

cc

cc F

F FF

aca

acc

bc

AA

AA A

AAA

New Guinea origin

Expansion to Asia

Diversification within New Guinea

Diversificationwithin Oceania

50 40 30 20 10 0

no crown"red" crownwhite crownblue crowngrey crown

P. p. f

rate

r

P. rar

oton

gens

is

P. cor

alen

sis

P. cha

lcuru

s

P. ins

ular

is

P. hut

toni

P. per

ousii

P. por

phyr

aceu

s

P. por

phyr

aceu

s

P. gre

yiP. r

osei

capi

lla

P. rich

ards

ii

P. pel

ewen

sis

P. pur

pura

tus

P. p. c

hrys

ogas

ter

P. dup

etith

ouar

sii

P. mer

cierii

P. reg

ina

P. cor

onul

atus

P. mon

acha

P. viri

dis

P. eug

enia

eP. i

ozon

us

P. per

latu

s

P. aur

antiif

rons

P. orn

atus

P. wal

lacii

P. hyo

gast

rus

P. tan

nens

is

P. sol

omon

ensis

P. rivo

liP. s

uper

bus

P. por

phyr

eus

P. cin

ctus

P. mel

anos

pilu

s

P. lut

eovir

ens

P. lay

ardi

P. vict

or

P. nai

nus

D. hol

oser

icea

A. pul

cher

rimus

P. mar

chei

P. mer

rilli

P. lec

lanc

heri

P. jam

bu

P. occ

ipita

lis

P. mag

nific

us

P. ber

nste

inii

D. aen

aD. p

acific

a

D. bico

lor

C. nico

baric

a

T. waa

liaT. v

erna

ns

P. pul

chel

lus

1

Highlights 2

Ptilinopus forms a clade that includes Alectroenas and Drepanoptila. 3 4

Basal divergences dated to the Early Oligocene. 5 6

Fruit doves originated most probably from the proto New Guinea region. 7 8

Colonization of Oceania was not associated with a significant increase of 9 diversification rate. 10

11

12

P. p. frater

P. rarotongensis

P. coralensis P. chalcurus

P. insularis P. huttoni P. perousii

P. p. ponapensis

P. porphyraceus P. greyi

P. roseicapilla P. richardsii P. pelewensis

P. purpuratus

P. p. chrysogaster

P. dupetithouarsii P. mercierii

P. regina P. coronulatus

P. monacha P. pulchellus

P. viridis P. eugeniae

P. iozonus P. perlatus P. aurantiifrons P. ornatus P. wallacii P. hyogastrus P. tannensis P. solomonensis P. rivoli P. superbus

P. porphyreus P. cinctus

P. melanospilus P. luteovirens P. layardi P. victor

P. nainus D. holosericea

A. pulcherrimus

P. marchei P. merrilli

P. leclancheri P. jambu P. occipitalis

P. magnificus P. bernsteinii

D. aena D. pacifica

D. bicolor

C. nicobarica T. waalia T. vernans

New Guinea origin

Expansion to Asia

Diversification within New Guinea

Diversificationwithin Oceania

50 40 30 20 10 0

Independant dispersals to Oceania

Ptlinopus Fruit doves

Phylogeny and biogeography of the fruit doves (Aves: Columbidae)

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