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Phylogenetic connections of phyllodinous species of Acacia
outside Australia are explained by geological history
and human-mediated dispersal
Gillian K. Brown
A,B
, Daniel J. Murphy
B,C
, James Kidman
A
and Pauline Y. Ladiges
A
A
School of Botany, The University of Melbourne, Vic. 3010, Australia.
B
National Herbarium of Victoria, Royal Botanic Gardens Melbourne, Vic. 3141, Australia.
C
Corresponding author. Email: daniel.murphy@rbg.vic.gov.au
Abstract. Acacia sensu stricto is found predominantly in Australia; however, there are 18 phyllodinous taxa that occur
naturally outside Australia, north from New Guinea to Indonesia, Taiwan, the Philippines, south-western Pacific (New
Caledonia to Samoa), northern Pacific (Hawaii) and Indian Ocean (Mascarene Islands). Our aim was to determine the
phylogenetic position of these species within Acacia, to infer their biogeographic history. To an existing molecular dataset
of 109 taxa of Acacia, we added 51 new accessions sequenced for the ITS and ETS regions of nuclear rDNA, including
samples from 15 extra-Australian taxa. Data were analysed using both maximum parsimony and Bayesian methods. The
phylogenetic positions of the extra-Australian taxa sampled revealed four geographic connections. Connection A, i.e.
northern Australia–South-east Asia–south-western Pacific, is shown by an early diverging clade in section Plurinerves,
which relates A. confusa from Taiwan and the Philippines (possibly Fiji) to A. simplex from Fiji and Samoa. That clade is
related to A. simsii from southern New Guinea and northern Australia and other northern Australian species. Two related
clades in section Juliflorae show a repeated connection (B), i.e. northern Australia–southern New Guinea–south-western
Pacific. One of these is the ‘A. auriculiformis clade’, which includes A. spirorbis subsp. spirorbis from New Caledonia and the
Loyalty Islands as sister to the Queensland species A. auriculiformis; related taxa include A. mangium,A. leptocarpa and
A. spirorbis subsp. solandri. The ‘A. aulacocarpa clade’includes A. aulacocarpa,A. peregrinalis endemic to New Guinea,
A. crassicarpa from New Guinea and Australia, and other Australian species. Acacia spirorbis (syn. A. solandri subsp.
kajewskii) from Vanuatu (Melanesia) is related to these two clades but its exact position is equivocal. The third biogeographic
connection (C) is Australia–Timor–Flores, represented independently by the widespread taxon A. oraria (section
Plurinerves) found on Flores and Timor and in north-eastern Queensland, and the Wetar island endemic A. wetarensis
(Juliflorae). The fourth biogeographic connection (D), i.e. Hawaii–Mascarene–eastern Australia, reveals an extreme disjunct
distribution, consisting of the Hawaiian koa (A. koa,A. koaia and A. kaoaiensis), sister to the Mascarene (Réunion Island)
species A. heterophylla; this clade is sister to the eastern Australian A. melanoxylon and A. implexa (all section Plurinerves),
and sequence divergence between taxa is very low. Historical range expansion of acacias is inferred to have occurred several
times from an Australian–southern New Guinean source. Dispersal would have been possible as the Australian land mass
approached South-east Asia, and during times when sea levels were low, from the Late Miocene or Early Pliocene. The close
genetic relationship of species separated by vast distances, from the Indian Ocean to the Pacific, is best explained by dispersal
by Austronesians, early Homo sapiens migrants from Asia.
Received 15 August 2012, accepted 29 October 2012, published online 14 December 2012
Introduction
Acacia Mill. sensu stricto (Leguminosae subfam. Mimosoideae),
formerly Acacia subgen. Phyllodineae DC (Maslin 2008), is
the largest genus of vascular plants in Australia, represented
by ~1045 species when undescribed taxa are included (Maslin
2004; Lewis et al.2005). Ninety per cent of the taxa within
the genus have phyllodinous leaves, with the remainder (in
two sections, Botrycephalae and Pulchellae) having bi-pinnate
foliage (Pedley 1975; Maslin 2001a). The distribution of
Acacia is predominantly Australian, where the genus is
dominant in semiarid and arid vegetation, although the highest
species diversity is in the south-west of Western Australia and
along the Great Dividing Range of eastern Australia (Maslin
2001a; Murphy et al.2010). In addition, 17 species and two
subspecies occur in four regions outside the Australian continent
(Pedley 1975,1990; Table 1, Fig. 1). All of these extra-Australian
species are phyllodinous and, on the basis of morphology,
are currently classified in sections Juliflorae and Plurinerves
(Maslin 2001a). However, there has been no molecular-
based analysis of the phylogenetic position of all of these
species as a test of their classification and to inform their
biogeographic history.
Journal compilation ÓCSIRO 2012 www.publish.csiro.au/journals/asb
CSIRO PUBLISHING
Australian Systematic Botany, 2012, 25, 390–403
http://dx.doi.org/10.1071/SB12027
Table 1. Acacia taxa sampled for the study, and added to specimens from Murphy et al.(2010)
Seedling accessions are shown as ‘cultivated’in the herbarium-source column. Species distribution, section (as per Maslin 2001a,2001b), DNA voucher number, locality information and GenBank numbersare
given. Sections: J, section Juliflorae; Pl, section Plurinerves. Museums and herbaria: BISH, Bishop Museum; BRI, Queensland Herbarium; CANB, Australian National Herbarium;MEL, National Herbarium of
Victoria; MELU, University of Melbourne Herbarium; NY, New York Botanical Garden. Location abbreviations: Australia: NSW, New South Wales; NT, Northern Territory; Qld, Queensland; SA, South
Australia; Tas., Tasmania; Vic., Victoria; WA, Western Australia. PNG, Papua New Guinea. Dash indicates lack of sequence. Not sequenced: A. richii A.Gray, A. mathuataensis A.C.Sm.
Taxon Distribution Section Herbarium
or source
Accession
number
DNA # Locality ITS ETS
A. aulacocarpa Cunn. ex Benth. NSW, Qld J BRI AQ 578374 JK06 Qld, Moreton, Mount
Tundbubudla
JX997272 JX997220
A. auriculiformis A.Cunn. ex Benth. Maluku (Indonesia),
New Guinea, NT, Qld
J MEL GB/CP/MB 154 JK07 Qld, Atherton Arboretum.
Source: East Normanby
River
JX997273 JX997221
Cultivated (MELU) MELU D 105526 JK46 PNG, Mibini JX997274 JX997222
Cultivated (MELU) MELU D 105525 JK45 NT, south of Alligator
River
JX997275 JX997223
A. celsa Tindale Qld J MEL 2103117 JK27 Qld, Cooktown towards
Daintree
JX997276 JX997224
A. complanata A.Cunn. ex Benth. NSW, Qld Pl MEL 282085 JK34 Qld, Burnett, Abbeywood,
north-north-east of Proston
JX997277 JX997225
A. confusa Merr. Taiwan, northern
Philippines
Pl NY NY190114 JK08 Hawaii, Pu’u’ialaka’a
State Wayside Park,
cultivated
JX997278 JX997226
MEL Staples 1221 Z31 Hawaii JX997271 JX997219
A. cowleana Tate NSW, NT, Qld, WA J MEL 2308940 JK11 Qld, Burke, Old Myally
Homestead
JX997279 JX997227
A. crassicarpa M.W.McDonald &
Maslin
New Guinea, Qld J MEL GB/CP/MB 151 JK09 Qld, Atherton Arboretum.
Source: SFR607
JX997280 JX997228
Cultivated (MELU) MELU D 105528 JK48 PNG, Morehead West JX997281 JX997229
Cultivated (MELU) MELU D 105527 JK47 Qld, South Coen Cape
York
JX997282 JX997230
A. disparrima subsp. calidestris M.W.
McDonald & Maslin
Qld J Cultivated (MELU) MELU D 105530 JK49 Qld, Garioch JX997283 JX997231
MEL (ex-BRI #) AQ742665 Z166 Qld, Undilla Station JX997284 JX997232
A. disparrima M.W.McDonald and
Maslin subsp. disparrima
NSW, Qld J Cultivated (MELU) MELU D 105529 JK41 Qld, north of Yeppon JX997285 JX997233
MEL 2220621 Z303 Qld, Gympie region, Imbil JX997286 JX997234
A. elachantha M.W.McDonald &
Maslin
NT, Qld, SA, WA J MEL 2287641 JK21 Qld, Cook, between
Lakeland and foothills of
Byrestown Range
JX997287 JX997235
A. excelsa Benth. NSW, Qld Pl MEL 1585525 JK12 Qld, North Kennedy,
Charters towers
JX997288 JX997236
A. heterophylla Willd. Mascarene Islands Pl BRI AQ598033 JK01 Réunion Island JX997289 JX997237
A. holosericea A.Cunn ex G.Donn. NT, Qld, WA J MEL 246766 JK16 NT, Gulf of Carpenteria,
Koolatong River
JX997290 JX997238
A. implexa Benth. NSW, Qld, Vic., Tas. Pl MEL 2083119 JK63 Qld ‘Toondahra’Paddy’s
Gully paddock
JX997291 JX997239
A. kauaiensis Hilleb. Hawaii Pl BRI AQ518156 JK64 Hawaiian Islands JX997292 JX997240
Extra-Australian Acacia phylogeny and biogeography Australian Systematic Botany 391
Table 1. (continued )
Taxon Distribution Section Herbarium
or source
Accession
number
DNA # Locality ITS ETS
A. kaoia Hilleb. Hawaii Pl BISH 652754 JK56 Hawaii, Oahu, Waahila
Ridge
JX997293 JX997241
BISH 721029 JK57 Hawaii, Maui, Makawao
Forest Reserve
JX997294 JX997242
A. koa A.Gray Hawaii Pl BISH 640020 JK54 Hawaii, Kauai, Hanalei
District, Kalalau Valley
JX997295 JX997243
BRI AQ727463 JK55 Hawaii, Oahu JX997296 JX997244
A. lamprocarpa O.Schwarz WA J Cultivated (MELU) MELU D 105531 JK50 NT, 14 km south of
Maningrida
JX997297 JX997245
A. leptocarpa A.Cunn. ex. Benth. New Guinea, NT, Qld, WA J BRI AQ 766661 JK02 Qld, North Kennedy,
Gunnawara
JX997298 JX997246
Cultivated (MELU) MELU D 105533 JK59 PNG, Kiriwo JX997299 JX997247
Cultivated (MELU) MELU D 105532 JK58 NT, Annie Creek JX997300 JX997248
A. mangium Willd. Maluku (Indonesia) New
Guinea Qld
J Cultivated (MELU) MELU D 105534 JK60 Qld, 7 km south-south-east
of Mossman
JX997301 JX997249
Cultivated (MELU) MELU D 105535 JK42 PNG, Aiambak Fly River
western province
JX997302 JX997250
A. melanoxylon R.Br. NSW, Qld, Vic., SA, Tas. Pl MEL 2138780 JK66 NSW, southern
Tablelands, Lake
Burrinjuck
JX997303 JX997251
MEL 2066689 JK67 Vic., eastern Highlands,
Dodd Street Reserve
JX997304 JX997252
A. midgleyi M.W.McDonald & Maslin Qld J Cultivated (MELU) MELU D 105536 JK43 Qld, Old Lockhart JX997305 JX997253
Cultivated (MELU) MELU D 105537 JK44 Qld, Old Lockhart JX997306 JX997254
A. multisiliqua (Benth.) Maconochie NT, Qld, WA Pl MEL 2036270 JK29 NT, Victoria River,
Gregory National Park
JX997307
A
JX997255
BRI 718050 JK30 Qld JX997308 JX997256
A. oraria Muell. Flores, Timor, Qld Pl MEL GB165 JK10 Qld, on slip road to
Mowbray River off
Captain Cook Highway
JX997309 JX997257
A. peregrinalis M.W.McDonald
& Maslin
New Guinea J CANB 358184.1 JK68 PNG,2 km north of Woroi,
Oriomo River
JX997310 JX997258
A. pubirhachis Pedley Qld, PNG J MEL 252757 JK17 Qld, 4 km east of Hopevale
to Starke Road, on the track
to the mouth of the McIvor
River
JX997311 JX997259
MEL 2308927 JK18 East of Mata village (on
road to Dimisisi), western
Province, PNG
JX997312 JX997260
A. ramiflora Domin Qld Pl MEL 2233881 JK38 Qld, North Kennedy,
Lumholtz National Park
JX997313 JX997261
A. simplex (Sparrman) Pedley Tonga, Samoa, Fiji, New
Caledonia, Vanuatu
Pl MEL MJB2069 Z358 New Caledonia JX997314 JX997262
A. simsii M.W.McDonald & Maslin New Guinea, NT, Qld Pl Cultivated (MELU) MELU D 105539 JK62 PNG, Mata JX997315 JX997263
Cultivated (MELU) MELU D 105538 JK61 Qld, Weipa JX997316 JX997264
392 Australian Systematic Botany G. K. Brown et al.
Nine of the extra-Australian taxa occur also in northern
Australia (A. auriculiformis,A. crassicarpa,A. leptocarpa,
A. mangium,A. oraria,A. pubirhachis,A. sericoflora,
A. simsii and A. spirorbis subsp. solandri), and either New
Guinea (seven of these species shared) or Indonesia (three
species shared, Fig. 2). Of the other species in close proximity
to Australia, one is endemic to New Guinea (A. peregrinalis,
Fig. 2A), one is endemic to Timor (A. wetarensis, Fig. 2C), one is
more widespread, on Flores, Timor and Cape York (A. oraria,
Fig. 2A) and one occurs in the Philippines and Taiwan
(A. confusa, Fig. 2B). Five taxa are recorded for the south-
western Pacific (Fig. 3A), including Vanuatu, New Caledonia
and the Loyalty Islands (A. spirorbis subsp. spirorbis, including
A. solandri subsp. kajewskii), Fiji and the New Hebrides
(A. simplex,A. richii, possibly synonomous with A. confusa,
and A. mathuataensis, only known from the type specimen
from 1947) and Samoa (A. simplex). Wagner et al.(1990)
recorded three species (A. koa,A. koaia and A. kaoaiensis) for
the northern Pacific on the Hawaiian Islands (Fig. 3B), although
these are also considered under a wider concept of A. koa. One
species (A. heterophylla; synonym A. xiphoclada, Du Puy et al.
2002) occurs far west in the Indian Ocean on Madagascar
(introduced) and the Mascarene Islands (endemic) (Fig. 1). It
has been hypothesised that A. koa is closely related to the
Australian species A. melanoxylon (Rock 1913; Pedley 1975;
Wagner et al.1990) and to the Réunion Island endemic
A. heterophylla (Vassal 1969; Pedley 1975).
Some of the extra-Australian acacias are of interest also
because of their importance in tropical agroforestry, being
used for timber, fuel wood, land rehabilitation and pulp for
paper manufacturing (McDonald et al.2001). Research into
growth rates, population genetics and dynamics, hybridisation
and silviculture have highlighted the use of acacias for
international timber production (Turnbull 1984; Moran et al.
1989a,1989b; Turnbull et al.1998;Yu2007). Large plantations
of A. mangium,A. auriculiformis,A. crassicarpa and
A. peregrinalis are grown commercially in Indonesia
and Malaysia (Turnbull et al.1998). The most widely studied
extra-Australian species is the Hawaiian A. koa (e.g. Harrington
et al.1995; Daehler et al.1999; Ares et al.2000; Pearson and
Vitousek 2001; Baker et al.2008). Traditionally, the wood of
A. koa has been used for canoes and huts by native Hawaiians,
and it is widely used in western countries for furniture and
musical instruments.
Our interest in determining the phylogenetic position of
the extra-Australian species of Acacia is to provide a basis for
understanding their geographic distributions and connections.
It is hypothesised that their evolutionary history is associated
with two processes. First, distribution of clades may correlate
with geological history. As the Australian and New Guinea land
mass moved northwards in the Neogene and came into close
proximity with South-east Asia and island archipelagos (e.g. Hall
1998,2009), range expansion would have been possible, as
inferred for various taxa, including close relatives of Acacia,
Paraserianthes (Brown et al.2011), and other Australian plant
groups that include extra-Australian species, such as in
Eucalyptus (Ladiges et al.2003). Second, distributions of taxa
may relate to more recent anthropogenic processes, where people
have carried plant material. The movement and distribution of
A. spirorbis subsp. solandri, syn
A. solandri subsp. kajewski Pedley
Vanuatu J BRI AQ719024 JK53 French Polynesia JX997317 JX997265
subsp. spirorbis Pedley New Caledonia MEL MJB2121 Z359 New Caledonia JX997318 JX997266
MEL MJB2056 Z360 New Caledonia JX997319 JX997267
subsp. Solandri (Benth.) Pedley Qld J MEL 2295855 JK32 Qld, North Kennedy,
Mount Inkerman
JX997320
B
JX997268
A. tropica (Maiden & Blakely) Tind. NT, Qld J MEL 292920 JK39 Qld, Burke, Murray
Springs
JX997321 JX997269
MEL 281520 JK40 Qld, Burke, Musselbrook
Mining Camp
JX997322
A
JX997270
A. wetarensis Pedley Wetar, Indonesia J BRI AQ513257 JK03 Wetar, Ilwaki JX997323
Outgroups
Paraserianthes lophantha (Willd.)
I.C.Nielsen
South-western WA N/A MEL MEL2057862 –Vic., Phillip Island EF638203 EF638105
Falcataria toona (Bailey) G.K.
Brown, D.J.Murphy & P.Y.Ladiges
North-eastern Qld N/A CANB CANB367091 Z77 Qld, North Kennedy,
Proserpine
EF638205 EF638107
A
ITS1 sequenced.
B
ITS2 sequenced.
Extra-Australian Acacia phylogeny and biogeography Australian Systematic Botany 393
early human colonists in the Australasian and Pacific regions
has been widely studied (e.g. Diamond 2000; Gray and Jordan
2000; Athens et al.2004; Trejaut et al.2005; Larson 2007;
Regueiro et al.2008), and traditional uses of Acacia are
known for Australian indigenous people (Kean 1991) and
native Hawaiians (Whitesell 1964).
Materials and methods
A total of 34 taxa, 17 of which were of extra-Australian origin,
was sampled for sequencing ribosomal nuclear DNA regions
ITS and ETS (Table 1, which includes taxon authorities). These
taxa were represented by 74 accessions, and the sequences
were added to an existing dataset of 109 taxa in Acacia
(Murphy et al.2010). Only three of the extra-Australian
species, including two from Fiji, namely, A. richii (or syn.
A. confusa) and A. mathuatensis, and A. sericoflora from
Papua New Guinea, were unable to be sampled. Outgroup taxa
of tribe Ingeae, which is sister to tribe Acacieae, were also
sampled, and two outgroups were selected to include the
closest relatives, Paraserianthes lophantha and Falcataria
toona, on the basis of higher-level analyses (Brown et al.2011).
Total genomic DNA was isolated from 20 mg of dry leaf
material with the QIAGEN DNeasy Plant Mini Kit, following
the manufacturer’s protocol (QIAGEN, Valencia, CA, USA). The
external (ETS) and internal (ITS) transcribed spacer regions
(ETS) of nuclear rDNA (nrDNA) were amplified from purified
DNA by using polymerase chain reaction (PCR). The ETS
region was amplified using primers AcR2 (Ariati et al.2006)
and 18SIGS (Baldwin and Markos 1998), and the ITS was
amplified using S3, S5, S6 (Käss and Wink 1997) and 26SE
(Sun 1994).
Recalcitrant PCR templates were amplified with the
addition of DMSO (dimethyl sulfoxide) to the PCR mixture.
PCR products were then purified using QIAquick PCR
Purification Kit (QIAGEN), as per manufacturer’s protocol.
Direct sequencing was accomplished with the same forward
and reverse PCR primers, by using ABI Prism BIG Dye
Terminator Cycle Sequencing Ready Reaction Kits (Perkin-
Elmer, Applied Biosystems, Foster City, CA). Sequence
reactions were separated and analysed at the Australian
Genome Research Facility.
Contiguous sequences were edited with Sequencer v. 4.8
(Gene Codes Corporation, Ann Arbor, MI) and manually
aligned in Bioedit sequence-alignment editor v. 7.0.9.0 (Hall
1999). Any uncertain base positions and highly variable regions
with uncertain sequence homology were excluded from
phylogenetic analyses. Individual base positions were coded as
unordered multistates; insertions–deletions (indels) were coded
as binary or unordered multistate characters and included as a
separate data partition in Nexus-formatted files for phylogenetic
analysis. Sequences are available in GenBank and alignments
from the authors on request.
Phylogenetic analyses
Parsimony analysis of aligned and coded sequences was
implemented using PAUP v. 4.0b10 (Swofford 2002).
Analysis of ITS and ETS regions separately showed no
incongruence and thus the regions were combined for the
analysis presented here. Characters were treated as unordered
and of equal weight. Heuristic searches were carried out
using 1000 random stepwise additions by using the tree–
bisection–reconnection method (TBR), saving 1000 trees per
replicate. A strict consensus tree was constructed of the set of
most parsimonious trees. Bootstrap support values were
calculated on the basis of 1000 bootstrap replicates, with 10
random stepwise additions per replicate and 500 trees saved
per replicate.
A
B
D
C
Fig. 1. Phyllodinous species of Acacia that occur outside Australia are found in four regions. A. South-east Asia
(Taiwan and Philippines), Indonesia (Flores, Timor, southern Moluccas) and New Guinea, some taxa ofwhich also
occur in northern Australia. B. New Caledonia, Loyalty Islands, Vanuata, Fiji and Samoa in the south-western
Pacific. C. Hawaiian Islands in the northern Pacific. D. Madagascar (introduced) and Mascarene Islands (endemic)
in the Indian Ocean.
394 Australian Systematic Botany G. K. Brown et al.
Bayesian analysis was performed using MrBayes version
3.1.2 (Ronquist and Huelsenbeck 2003). Sequence data were
divided into six partitions, with the ITS region being divided into
four partitions, including ITS1, 5.8S, ITS2 and LSU, and the
ETS region being divided into two partitions, including SSU
and ETS. A separate GTR + I + gamma model was applied to
each of the sequence-data partitions. Multistate indel characters
were included as a separate data partition, and to this partition, a
standard discrete-state model with a gamma-shape parameter
was applied. A Markov chain Monte Carlo search was run for
8 million generations, with trees sampled every 100 generations.
Two simultaneous analyses were performed starting from
different random trees (Nruns = 2), each with four Markov
chains (Nchains = 4). The first 20 001 trees were discarded
from each run as the burn-in. A Bayesian consensus
phylogram and posterior probability (PP) values for each node
were calculated in MrBayes.
Results
The multiple sequence alignment of ITS and ETS sequences when
concatenated consisted of 1290 base pairs. In addition, eight indel
characters, six from the ITS region and two from the ETS region,
were scored as multistate characters. Analyses using all outgroups
from tribe Ingeae (not presented), confirmed the finding of Brown
et al.(2011) that Paraserianthes lophantha is the sister taxon to
Acacia.
The MP analysis of the combined ITS and ETS dataset resulted
in 7000 trees of length 2515 steps and consistency index of 0.382.
The Bayesian analysis gave a similar tree topology but had more
nodes resolved. The structure of the Bayesian tree, highlighting
major clades in Acacia and the position of the extra-Australian
taxa, is shown in Fig. 4, with full details given in Fig. S1, available
as Supplementary material. Nodes not resolved in the MP strict
consensus tree are indicated by an asterisk, and branches at nodes
AB
CD
Fig. 2. Distributions of Acacia taxa in the Australasian region. A. Acacia perigrinalis endemic to southern New Guinea; A. oraria
endemic to Flores, Timor and north-eastern Queensland. B. Acacia mangium, southern New Guinea, southern Moluccas and Cape
York; A. confusa, Taiwan and the Philippines, and possibly (as A. richii) in Fiji. C. Acacia spirorbis subsp. solandri endemic to eastern
Queensland; A. crassicarpa southern New Guinea, Cape York and eastern Queensland; A. pubirhachis, southern New Guinea and
Cape York; A. wetarensis endemic to Timor. D. Overlapping distributions of three species that occur in both southernNew Guinea and
northern Australia: A. auriculiformis (also Kei Islands, southern Moluccas), A. leptocarpa (also eastern Queensland) and A. simsii.
Extra-Australian Acacia phylogeny and biogeography Australian Systematic Botany 395
with PP 0.95 support are indicated by thick lines (Fig. 4).
Details of the clades that include the extra-Australian taxa are
shown in Figs 5–7. Multiple accessions of the same species
clustered together, with the exception of A. spirorbis,A. koa
and A. disparrima (see below).
At the lower nodes of the Acacia phylogram (Fig. 4), there
are four strongly supported lineages at Nodes 2, 3, 5 and 6,
all with PP = 1.00. The first of these lineages, labelled Clade 1
(Node 2, Figs 4,5), includes three of the extra-Australian species,
namely, A. confusa,A. simplex and A. simsii. Clade 1 is possibly
the sister group (at Node 1, PP =0.86) to the second lineage, the
A. victoriae–A. pyrifolia clade (Node 3), which has been
identified previously as an early divergence within the
Australian acacias (Murphy et al.2010). The third lineage is
the ‘Pulchelloidea’clade of species mostly from Western
Australia (Node 5), also previously resolved in Murphy et al.
(2010). The fourth lineage (Node 6) includes the A. murrayana
clade (Node 7, PP = 0.97) and its sister group, the large ‘p.u.b.
clade’(Node 8, PP = 1.00). The ‘p.u.b. clade’includes section
Plurinerves, most of section Phyllodineae (uninerved phyllodes)
and section Botrycephalae, and it is estimated to include 80–90%
of species diversity in Acacia (Murphy et al.2010). The other
extra-Australian species are positioned within the ‘p.u.b. clade’,
as part of the polytomous Node 12 (Fig. 4).
The phylogram (Fig. 4) thus shows that the extra-Australian
species of Acacia are polyphyletic and placed within five clades
(Figs 5–7). Relationships of taxa within these clades indicate
four geographic patterns, as follows: (A) northern Australia–
South-east Asia–south-western Pacific connection; (B) northern
Australia–New Guinea–south-western Pacific connection; (C)
northern Australia–Timor–Flores connection and (D) Hawaii–
Mascarene–eastern Australia connection.
A. Northern Australia–South-east Asia–south-western Pacific
connection;section Plurinerves
Clade 1 (Node 25, Fig. 5) reveals geographic pattern (A), which is
a connection between Australia, South-east Asia and the south-
western Pacific. Acacia confusa, the species from Taiwan and the
Philippines (and possibly Fiji if synonymous with A. richii), is
related to A. simplex found in Fiji and Samoa. This group is related
to A. multisiliqua, which is scattered across northern Australia
from the northern Kimberley to Arnhem Land and offshore
islands, and a clade (PP = 1.00) of A. simsii from Australia and
New Guinea (northern, eastern and western coasts; Pedley 1975)
and two Queensland species, A. complanata and A. ramiflora.
Also related to these species (PP = 1.00) is A. excelsa, which
occurs in southern inland Queensland and New South Wales. All
of these taxa are in section Plurineves and have been considered
to be more or less related (see Cowan and Maslin 2001, e.g.
p. 135). Branch lengths in the phylogram (Figs 4,5) show large
divergences among taxa. Of interest is the sister relationship
(PP =1.00) of the Western Australian A. longispinea to Clade 1.
B. Northern Australia–southern New Guinea–south-western
Pacific connection;section Juliflorae
Clades 2 and 3 (Fig. 6) are both in section Juliflorae, a section
supported by morphology (e.g. spicate inflorescences). However,
in our analysis, the taxa sampled from Juliflorae, including Clades
2 and 3, are part of an unresolved polytomy, at Node 15, with weak
support (PP = 0.51). Nonetheless, Clade 2 (Node 16, PP = 0.97)
provides evidence of a link between northern Australia and
southern New Guinea, whereas Clade 3 (Node 17, PP = 0.71)
links northern Australia and southern New Guinea (and southern
Moluccas) to New Caledonia and the Loyalty Islands, south-
western Pacific. Acacia spirorbis from Vanuatu (A. spirorbis FP,
Fig. 6, which is equivalent to A. solandri subsp. kajewskii, Pedley
1975), is related to these taxa at Node 15. Also at this polytomous
node is A. pubirharchis, which extends from Queensland to the
western province of Papua New Guinea.
Clade 2 is the ‘A. aulacocarpa group’with the New Guinea
endemic A. peregrinalis related most closely to two Queensland
taxa, A. disparrima subsp. calidestris (PP = 1.00) and A. celsa
(PP = 0.72, Fig. 6). They are related as a group to A. midgleyi
from New Guinea (PP = 1.00) and A. aulacocarpa (0.97) from
Queensland. Also in Clade 2, with relationships unresolved, are
A. crassicarpa, another species that occurs in both New Guinea
A. spirorbis =
A. solandri subsp.
kajewskii A. simplex
A. spirorbis subsp. spirorbis
A. richii &
A. mathuataensis
160
°
180
°
Vanuatu
Fiji
Loyalty Is.
New Caledonia
Samoa
170
°
W
170
°
E
20
°
S
18
°
A. koa
A. kauaiensis
A. koaia
Hawaii
Maui
Molokai
Oahu
Kauai
Lanai
155
°
W
22
°
N
20
°
14
°
AB
Fig. 3. Distributions of Acacia taxa in the Pacific region. A. South-western Pacific: New Caledonia and Loyalty Islands: A. spirorbis subsp. spirorbis; Vanuatu:
A. spirorbis subsp. solandri (syn. A. solandri subsp. kajewskii); Fiji: A. richii,A. mathuataensis and A. simplex. B. Northern Pacific, Hawaiian endemics: A. koa,
A. koaia and A. kauaiensis (this last taxon is also recognised as synonymous with A. koa; Adamski et al.2012).
396 Australian Systematic Botany G. K. Brown et al.
and Australia; A. disparrima subsp. disparrima from Queensland
and New South Wales; and A. lamprocarpa, which has a
distribution disjunct from the Queensland taxa, occurring
across northern Australia, from the Kimberley to the Gulf region.
Clade 3 (Fig. 6) is the ‘A. auriculiformis group’.
Acacia auriculiformis (three accessions) and A. mangium (two
accessions), both of which occur in northern Australia, New
Guinea and Indonesia (southern Moluccas), are related to
Acacia spirorbis subsp. spirorbis (two accessions, PP = 0.79)
found in New Caledonia and the Loyalty islands. These taxa are
related to northern Australian species A. cowleana,A. elachantha,
A. holosericea,A. leptocarpa (also in southern New Guinea),
A. spirorbis subsp. solandri and A. tropica.
C. Australia–Timor–Flores connection;section Plurinerves
The biogeographic connection between Australia and Indonesia
is represented in our analysis by the widespread distribution of
Fig. 4. Overview of the Bayesian phylogram of Acacia based on the combined ITS and ETS datasets, showing positions
of major clades and extra-Australian taxa (green). Posterior probability (PP) support values are shown in italic for the main
nodes, which are also numbered; branches with 0.95 probability support are shown as thick lines, and levels of taxon
divergence are indicated by mean branch lengths. Nodes that were unresolved in the maximum parsimony strict consensus
tree are indicated by an asterisk; red circles indicate relationships that differ from the maximum parsimony strict consensus
tree. Detailed tree with all taxa labelled is given in Fig. S1.
Extra-Australian Acacia phylogeny and biogeography Australian Systematic Botany 397
A. oraria (section Plurinerves) sampled from north-eastern
Queensland, but which occurs also on the islands of Flores
and Timor. Clade 4 (Node 18, Fig. 7A) shows A. oraria as
related to A. dawsonii from eastern Australia (PP = 1.00), an
unexpected result considering differences in morphology.
Maslin (2001b) described A. oraria as ‘seemingly related to
A. melanoxylon’.Acacia oraria and A. dawsonii are shown
related to (PP = 0.90), but widely divergent from, sister species
A. dictyoneura and A. leptalea (PP = 0.97), both from south-
western Western Australia.
D. Hawaii–Mascarene–eastern Australia;section Plurinerves
Geographic pattern D is revealed from Clade 5 (Node 22,
Fig. 7B), with all resolved nodes strongly supported
Clade 1, node 25 N Aust.–SE Asia–SW Pacific
1.00
1.00
0.59*
1.00
1.00 1.00
1.00
1.00*
0.1
A. longispinea
1.00
1.00
JK12 A. excelsa QL JK29 A. multisiliqua
JK30 A. multisiliqu
a
Z358 A. simplex
Z31 A. confusa A. confusa
JK62 A. simsii PNG
JK61 A. simsii QL
JK34 A. complanata QL
JK38 A. ramiflora QL
2
25
Fig. 5. Details of Clade 1, section Plurinerves (Fig. 4), which show a northern Australia–south-eastern Asia–south-
western Pacific connection (Pattern A, from Node 25). PNG, Papua New Guinea; and QL, Queensland. Posterior
probabilities are shown in italic at nodes.
0.70
0.88
1.00
0.72
1.00
1.00
0.97
1.00
0.53
0.97
1.00
1.00
0.55
1.00
0.95
0.79
0.59
0.96
0.71
0.51
*
*
*
*
*
*
*
*
*
*
Clade 2, node 16
A. aulacocarpa group
N Aust.–S New Guinea
Clade 3, node 17
A. auriculiformis group
N Aust.–S New Guinea–SW Pacific
15
17
A. rossei
A. genistifolia
JK53 A. spirorbis FP
A. cincinnata
A. dimidiata
JK50 A. lamprocarpa NT
JK09 A. crassicarpa QL
JK47 A. crassicarpa QL
JK48 A. crassicarpa PNG
JK06 A. aulacocarpa QL
JK27 A. celsa QL
Z166 A. disparrima subsp. calidestris QL
JK49 A. disparrima subsp. calidestris QL
16
JK68 A. peregrinalis PNG
JK43 A. midgleyi QL
JK44 A. midgleyi QL
JK41 A. disparrima subsp. disparrima QL
Z303 A. disparrima subsp. disparrima QL
JK18 A. pubirharchis PNG
JK17 A. pubirharchis QL JK16 A. holosericea NT
JK21 A. elachantha QL
JK40 A. tropica QL
JK39 A. tropica QL
JK11 A. cowleana QL
JK32 A. spirorbis subsp. solandri QL
JK02 A. leptocarpa QL
JK58 A. leptocarpa NT
JK59 A. leptocarpa PNG
JK42 A. mangium PNG JK60 A. mangium QL
JK45 A. auriculiformis NT
JK07 A. auriculiformis QL
JK46 A. auriculiformis PNG
Z359 A. spirorbis subsp. spirorbis NC
Z360 A. spirorbis subsp. spirorbis NC
0.1
Fig. 6. Details of Clades 2 and 3, section Juliflorae (Fig. 4), which show a northern Australia–southern New Guinea–south-
western Pacific connection (Pattern B). FP, French Polynesia; NC, New Caledonia; QL, Queensland; PNG, Papua New Guinea;
and NT, Northern Territory.
398 Australian Systematic Botany G. K. Brown et al.
(PP = 1.00). Clade 5 includes the monophyletic group of
accessions attributed to A. kaoia,A. kauaiensis and A. koa
from Hawaii and their sister species A. heterophylla from
Réunion Island (Mascarene Islands; and putatively introduced
to Madagascar). The Hawaiian and Mascarene clade is related to
two south-eastern Australian taxa, A. melanoxylon and A. implexa
(Fig. 7B), a relationship that has been inferred previously on the
basis of molecular and morphological evidence (see Miller et al.
2011).
The sequences for the Hawaiian and Mascarene accessions are
very similar to one another and to the Australian species, pointing
to recent geographic connection. Recently, Adamski et al.(2012)
also reported that ITS rDNA and chloroplast DNA (trnK intron)
sequences do not distinguish representative samples of the
Hawaiian ‘koa types’. However, they could separate A. koa,
A. koaia and intermediate forms on the basis of microsatellite
data, providing evidence of a level of genetic divergence, which
they conclude is consistent with taxonomic recognition of
subspecies within a single species. The genetic distance among
forms was not correlated with geographic distance among the
Hawaiian Islands, and genetic differentiation may be the result
of decreased population size (e.g. habitat loss) and genetic drift
(Adamski et al.2012).
Discussion
Phylogenetic relationships and taxonomy
The overall phylogeny supports previous results and the
informally named clades of Murphy et al.(2003,2010) and
Miller et al.(2003), confirming that the sections of Pedley
(1978) are not monophyletic. There is some additional
resolution in the previously identified ‘p.u.b clade’of Murphy
et al.(2010), although strong support is lacking for many of the
relationships within that clade. Although we consider section
Juliflorae to be monophyletic on the basis of the apomorphic
morphological character presence of spicate inflorescences, it
is not resolved as monophyletic on the basis of our molecular
data. With the exception of A. longifolia of section Juliflorae at
Node 12, most of the juliflorous taxa are grouped at Node 14, but
that node is a polytomy and includes some non-juliflorous taxa,
such as A. genistifolia (see Fig. S1). Because these nodes have
only low PP support, there remains the possibility that section
Juliflorae is monophyletic and that the species in Clades 2 and 3
are part of one lineage that had evolved before Australia came
into its more northerly position and which subsequently
differentiated, resulting in repeated biogeographic connections
outside Australia.
The results here suggest also that further taxonomic study
and sampling are needed to examine the monophyly of
some species, such as A. spirorbis and A. disparrima. Acacia
disparrima, for example, was previously considered to be part of
A. aulacocarpa sensu lato, a widespread, polymorphic complex,
which was split into several species and subspecies by McDonald
and Maslin (2000). More taxa may await discovery.
Biogeography: fossils and time frame
In Australia, Acacia pollen records date from the Late Eocene–
Earliest Oligocene. Oldest polyad records (37–34 million years
ago) are more generally ascribed to non-Acacia Mimosaceae,
tribe Ingeae (Macphail and Hill 2001; D. Cantrill, pers. comm.).
The most reliable records, however, are from the Late Oligocene;
such fossils are pollen polyads that have faces with distinctive
pseudocolpi (see illustrations in Macphail and Hill 2001). The
fossil Acaciapollenites, for example, is recorded from the Earliest
Oligocene in the Murray Basin, and also from the Late Oligocene
or Early Miocene in New Zealand (Macphail and Hill 2001).
These fossils thus provide a minimum age for Acacia and a time
frame for our discussion of biogeographic connections.
Northern Australian–southern New Guinean distributions
The seven extant species with distributions in northern Australia
and southern New Guinea were presumably contiguous
across that region, on the one landmass that is now fragmented
by the Gulf of Carpentaria and shallow Arafura Sea. One species,
A. peregrinalis, evolved as an endemic in southern New Guinea.
Major changes in sea level occurred during Quaternary glacial
cycles, with sea level being as low as –120 to –140 m during
glacial maxima and +5 to +8 m during the warmest interglacials,
compared with the present-day level (Hope et al.2004; Bowman
et al.2010). Periods of low sea level exposed continental shelf,
which resulted in land connections between southern New Guinea
and northern Australia and allowed the possibility of gene flow
between populations.
Range expansion beyond New Guinea
The historical range expansion of Acacia from an Australian–
southern New Guinean source into regions beyond is inferred to
have occurred several times, after major clades had evolved and
Australia had drifted northward, bringing it into contact with
South-east Asia–Melanesia. It is difficult to be certain about
1.00
0.97
0.90
Clade 4, node 18
Aust.–Timor–Flores
0.1
1.00
1.00
1.00
1.00
Clade 5, node 22
Hawaii–Mascarene–E Aust.
A
B
18
22
A. dawsonii
A. oraria QL
A. leptalea
A. dictyoneur
a
A. implexa QL
DM210 A. melanoxylon VIC
JK66 A. melanoxylon NSW
JK67 A. melanoxylon VIC
JK55 A. koa H
Z30 A. koa H
JK56 A. kaoia H
JK57 A. kaoia H
JK64 A. kauaiensis H
JK01 A. heterophylla RI
JK54 A. koa H
Fig. 7. A. Details of Clade 4, section Plurinerves (Fig. 4), which shows a
northern Australia–Timor–Flores connection (Pattern C). B. Clade 5, section
Plurinerves, which shows a Hawaii–Mascarene–eastern Australia connection
(Pattern D). H, Hawaiian Islands; NSW, New South Wales; QL, Queensland;
RI, Réunion Island; and Vic., Victoria.
Extra-Australian Acacia phylogeny and biogeography Australian Systematic Botany 399
details of palaeogeography in this geologically complex region,
which experienced rapid changes in the Cenozoic (Hall 2009).
At c. 25 million years ago, the New Guinea passive margin
collided with the leading edge of the eastern Philippines–
Halmahera–New Guinea arc system (Hall 2001). The Late
Miocene (10 million years ago), however, may have been a
time when sufficient land was exposed and seas were very
shallow, allowing connections and range expansions (Hall
1998,2009). Dispersal routes across Taiwan–Philippines–
North Moluccas–New Guinea and South Moluccas–Sunda
Islands may have become available from the Early Pliocene
(5 million years ago; Hoły
nska and Stoch 2012). The
Moluccas, for example, were elevated above sea level from
that time (Hall 2009). Biogeographic connections may also
relate to movement of Pacific terranes along the northern New
Guinea margin into the Moluccas and Philippines.
Among the acacias, the earliest range expansion is evidenced
by Clade 1 (Geographic pattern A), with A. confusa, found in
Taiwan and the Philippines, and A. simplex, in Fiji and Samoa,
related to a species in New Guinea (A. simsii) and northern
Australia (offshore islands and across northern Australia east
to Queensland and New South Wales; all in section Plurinerves).
Greater population sampling is needed to test whether A. confusa
occurs in Fiji and to test the taxonomic status of A. richii.
Although only known from the type specimen, A. mathuatensis
is thought to be related to A. simplex (Pedley 1975). With regard
to the history of the Fijian Acacia species, the Outer Melanesian
Island Arc could have provided a route, facilitated by low sea
level, for dispersal from Australasia onto Pacific Islands. The
Fijian Archipelago emerged in the Middle Miocene, and Vanuatu
and Fiji (also Tonga) were joined into a continuous island arc until
breakup in Mid–Late Miocene or Latest Miocene (5.5 million
years ago); the Samoan Islands, to which A. simplex extends, have
a different geological history, representing oceanic island
volcanism (Duffels and Ewart 1988).
Phylogenetic and biogeographic analyses of various taxa
have been published for the region of South-east Asia to the
western Pacific. For example, van Welzen et al.(2003) combined
data for 29 plant and animal groups to search for general patterns.
Using Brooks parsimony analysis, they presented a summary
area cladogram and network, showing relationships of areas east
of Weber’s Line as New Caledonia+Samoa ((Australia + New
Guinea) (Solomon Islands (Santa Cruz group (Vanuata
(Fiji + Tonga))))). De Boer (1995) concluded that cicadas of
the Indo-Pacific region show phylogenetic patterns congruent
with vicariance and geology involving movement of micro-
continents and fragmentation of island arcs. Paraserianthes
section Falcataria, which is related to Acacia and occurs in
tropical wet forest, follows a general track linking north-
eastern Australia to New Guinea, the Moluccas, the Bismarck
Archipelago and the Solomon Islands (Brown et al.2011).
Acacia section Juliflorae shows connections between
northern Australia–southern New Guinea and Melanesia in the
south-western Pacific (Geographic pattern B, Clades 2 and 3).
Related to, but outside Clades 2 and 3, is A. spirorbis subsp.
solandri (syn. A. solandri subsp. kajewskii) from Vanuatu;
however, A. spirorbis subsp. solandri from Queensland and
A. spirorbis subsp. spirorbis from New Caledonia are nested
within Clade 3. Acacia spirorbis is evidently not monophyletic
and the samples from different localities show different levels of
divergence (branch lengths). These data suggest the possibility of
different events and times of range expansion –one connection
through the East Melanesian arc to Vanuatu and another
connection between Australia–southern New Guinea and New
Caledonia. Long-distance dispersal to New Caledonia cannot be
discounted for Acacia (compared with vicariant explanations for
older taxa, such as argued for the eucalypt group; Ladiges and
Cantrill 2007). Long-distance dispersal has been inferred for
Acacia, e.g. from Australia to New Zealand, with seed having
the capacity to remain viable for a long time, survive in sea water
(see New 1984) and be attractive to migratory birds (Macphail and
Hill 2001).
Range expansion of Acacia to Indonesia needs further
investigation, with greater taxon sampling. The widespread
species A. oraria section Plurinerves, which extends from
north-eastern Queensland to Timor and Flores, needs sampling
across its geographic range to test our finding (on the basis of a
Queensland accession) that it is related to A. dawsonii and two rare
species from south-western Western Australia. If this pattern
is correct, the high degree of lineage divergence observed
implies that there has been some extinction between the south-
western and northern and eastern Australia, or that in this part of
the phylogeny, there remains unsampled phylogenetic diversity.
Furthermore, there is an endemic species on Timor and Flores
in section Juliflorae that was not included in the combined dataset.
Acacia wetarensis (Pedley 1975) was not sequenced for the ETS
region, but analysis of ITS alone (not shown) suggests that it is
related to the ‘A. aulacocarpa group’, Clade 2 described above, as
noted by McDonald and Maslin (2000). Thus, a biogeographic
connection between Australia and the Indonesian Archipelago,
including Timor, is evidenced by species in different sections of
Acacia as well as the sister taxon Paraserianthes lophantha
(Brown et al.2011). Timor is a young island that was elevated
rapidly above sea level in the past 3 million years after the
Australian margin collided with the Banda Volcanic Arc in
Timor c.3–4 million years ago (Hall 2009); thus, range
expansion is suggested to be from the Late Pliocene.
Anthropogenic dispersal
Clade 5 shows very close relationships among taxa separated by
vast distances, from the Indian Ocean to the northern Pacific.
Morphologically A. heterophylla (synonym A. xiphoclada;Du
Puy et al.2002) recorded for the Mascarene Islands resembles
A. koa sensu lato from Hawaii and A. melanoxylon from eastern
Australia. Pedley (1975) would have considered A. heterophylla
and A. koa conspecific if it were not for their great spatial
separation. Several studies have drawn links among these three
species through seed chemistry (Bell and Evans 1978), ploidy
level (Coulaud et al.1995) and morphology (Rock 1913; Vassal
1969; Pedley 1975). Both A. heterophylla and A. koa are
tetraploid, distinguishing them from A. melanoxylon, which is
diploid (Atchison 1948; Coulaud et al.1995). Carlquist (1965)
hypothesised that both A. koa and A. heterophylla are descendants
of seeds that floated into the Pacific and Indian Oceans from
Australia. Carlquist’s(1965) hypothesis, however, leaves
unsolved problems, such as the unexplained absence of similar
species from nearby islands (Pedley 1975), and why would
400 Australian Systematic Botany G. K. Brown et al.
dispersal occur from an eastern Australian acacia (aff.
A. melanoxylon) into the Indian Ocean rather than from one in
Western Australia? Bell and Evans (1978) argued that the
relationship between A. heterophylla and other Australian
phyllodinous species inferred that the relationship was
Gondwanan, i.e. that both Australia and the Mascarene Islands
once formed part of the same land mass. Such an old age is at odds
with the phylogeny and genetic similarity of these species
presented here.
Rather, the close genetic relationships of species separated
by vast distances, from the western Indian Ocean to the central
Pacific Ocean, is best explained by human-mediated dispersal
by Austronesians –early Homo sapiens migrants from Asia.
Austronesians include various populations that speak languages
of the Austronesian family, and include Taiwanese aborigines
and groups of people in the Philippines, Indonesia, Malaysia, East
Timor, Madagascar, Micronesia and Polynesia (New Zealand
and Hawaii). Gray and Jordan (2000), by using linguistics, and
Regueiro et al.(2008), by analysing autosomal short tandem-
repeat (STR) loci, presented models of the movement of people.
According to the out-of-Taiwan model, large-scale Austronesian
expansion from the region of Taiwan began c. 5000–2500 BC,
spreading south-east, then eastward, reaching the islands of
Melanesia by 1200 BC and Micronesia by 500 AD.
Austronesians also moved westward through Maritime South-
east Asia, eventually reaching Madagascar c. 400 AD. Regueiro
et al.(2008) also reported a connection between Australian and
Timor people and those in Madagascar. The alternative out-of-
Sundaland model (based on mitochondrial DNA lineages)
suggests that Austronesians were evolving within South-east
Asia for a longer period, dispersing when sea levels rose after
the last glacial maximum, 15 000–7000 years ago (Soares et al.
2008). Given either model of the origin of Austronesians, their
distribution, which extends from Madagascar to South-east Asia
to Oceania (Athens et al.2004), is congruent with the distribution
of those Acacia species that were probably valuable commodities
as fast-growing woody trees suitable for tools and ship-building.
Conclusions
Phylogenetic analysis of a large sample of Acacia has shown that
the taxa that occur beyond the Australian continent have
relationships within five different clades. The earliest dispersal
extended the range of Acacia, north to Taiwan and the Philippines
and east to Fiji and Samoa in the south-western Pacific. This
biogeographic track is suggested to date from the Late Miocene or
Early Pliocene and is correlated with the palaeogeographic
history of the region. Other range expansions were to Timor,
Vanuatu and New Caledonia. Seed dispersal is inferred in some
cases but processes for this are unknown. The distributions of
genetically very similar species, as far apart as Réunion Island
in the Indian Ocean and Hawaii in the northern Pacific, are
hypothesised to relate to the movement of Austronesian people.
Supplementary material
A Bayesian phylogram based on the combined ITS and ETS
datasets, showing position of all Acacia taxa sequenced and major
clades is available as Supplementary material from the journal
online (see http://www.publish.csiro.au/?act=view_file&file_id
=SB12027_AC.pdf).
Acknowledgements
We acknowledge funding from ARC Linkage grant LP0669625. We
gratefully acknowledge the directors and staff of the BISH, BRI, CANB,
MEL and NY herbaria for the loan of specimens used in this work.
References
Adamski DJ, Dudley NS, Morden CW, Borthakur D (2012) Genetic
differentiation and diversity of Acacia koa populations in the Hawaiian
islands. Plant Species Biology 27, 181–190.
doi:10.1111/j.1442-1984.2011.00359.x
Ares A, Fownes JH, Sun W (2000) Genetic differentiation of intrinsic water-
use efficiency in the Hawaiian native Acacia koa. International Journal
of Plant Sciences 161, 909–915. doi:10.1086/317559
Ariati SR, Murphy DJ, Udovicic F, Ladiges PY (2006) Molecular phylogeny
of three groups of acacias (Acacia subgenus Phyllodineae) in arid
Australia based on the internal and external transcribed spacer regions
of nrDNA. Systematics and Biodiversity 4, 417–426.
doi:10.1017/S1477200006001952
Atchison E (1948) Studies in the Leguminosae 2. Cytogeography of Acacia
(Tourn.) L. American Journal of Botany 35, 651–655.
doi:10.2307/2438145
Athens JS, Dega MF, Ward JV (2004) Austronesian colonization of
the Mariana islands: the paleoenvironmental evidence. Indo-Pacific
Prehistory Association Bulletin 24,21–30.
Baker PJ, Robinson AP, Ewel JJ (2008) Sudden and sustained response of
Acacia koa crop trees to crown release in stagnant stands. Canadian
Journal of Forest Research 38, 656–666. doi:10.1139/X07-137
Baldwin BG, Markos S (1998) Phylogenetic utility of the external transcribed
spacer (ETS) of 18S–26S rDNA: congruence of ETS and ITS trees of
Calycadenia (Compositae). Molecular Phylogenetics and Evolution 10,
449–463. doi:10.1006/mpev.1998.0545
Bell EA, Evans CS (1978) Biochemical evidence of a former link between
Australia and the Mascarene Islands. Nature 273, 295–296.
doi:10.1038/273295a0
Bowman DMJS, Braby MF, Brown GK, Brown J, Cook LG, Crisp MD, Ford
F, Haberle SG, Hughes J, Isagi Y, Joseph L, Ladiges PY, McBride J,
Nelson G (2010) Biogeography of the monsoon tropics: Australia’s last
biological frontier. Journal of Biogeography 37, 201–216.
doi:10.1111/j.1365-2699.2009.02210.x
Brown GK, Murphy DJ, Ladiges PY (2011) Relationships of the Australo-
Malesian genus Paraserianthes (Mimosoideae: Leguminosae) identifies
the sister group of Acacia sensu stricto and two biogeograhical tracts.
Cladistics 27, 380–390. doi:10.1111/j.1096-0031.2011.00349.x
Carlquist S (1965) ‘Island Life: a Natural History of the Islands of the World.’
(American Museum of Natural History, Natural History Press: Garden
City, NY)
Coulaud J, Brown SC, Siljak-Yakovlev S (1995) First cytogenetic
investigation in populations of Acacia heterophylla, endemic from La-
Réunion Island, with reference to A. melanoxylon. Annals of Botany 75,
95–100. doi:10.1016/S0305-7364(05)80013-7
Cowan R, Maslin BR (2001) ‘Flora of Australia. Vol. 11B.’(ABRS/CSIRO
Publishing: Melbourne)
Daehler CC, Yorkston M, Sun W, Dudley N (1999) Genetic variation in
morphology and growth characters of Acacia koa in the Hawaiian Islands.
International Journal of Plant Sciences 160, 767–773.
doi:10.1086/314163
De Boer AJ (1995) Islands and cicadas adrift in the West Pacific.
Biogeographic patterns related to plate tectonics. Tijdschrift voor
Entomologie 138, 169–244.
Extra-Australian Acacia phylogeny and biogeography Australian Systematic Botany 401
Diamond JM (2000) Taiwan’s gift to the world. Nature 403, 709–710.
doi:10.1038/35001685
Du Puy D, Labat JN, Rabevohitra R, Villiers J-F (2002) ‘The Leguminosae
of Madagascar.’(Royal Botanic Gardens, Kew: London)
Duffels JP, Ewart A (1988) The cicadas of the Fiji, Samoa and Tonga
Islands, their taxonomy and biogeography (Homoptera, cicadoidea).
Entomonograph 10,1–108.
Gray RD, Jordan FM (2000) Language trees support the express-train
sequence of Austronesian expansion. Nature 405, 1052–1055.
doi:10.1038/35016575
Hall R (1998) The plate tectonics of Cenozoic Southeast Asia and the
distribution of land and sea. In ‘Biogeography and geological
evolution of South-east Asia’. (Eds R Hall, JD Holloway) pp. 99–131.
(Backhuys Publishers: Leiden, the Netherlands)
Hall TA (1999) Bioedit: a user-friendly biological sequence alignment editor
and analysis program for Windows 95/98/NT. Nucleic Acids Symposium
Series 41,95–98.
Hall R (2001) Cenozoic reconstructions of SE Asia and the SW Pacific:
changing patterns of land and sea. In ‘Faunal and Floral Migrations
and Evolution in SE Asia–Australasia’. (Eds I Metcalfe, JMB Smith,
M Morwood, I Davidson) pp. 35–56. (AA Balkema Publishers: Lisse)
Hall R (2009) Southeast Asias’s changing palaeogeograhy. Blumea 54,
148–161. doi:10.3767/000651909X475941
Harrington RA, Fownes JH, Meinzer FC, Scowcroft PG (1995) Forest
growth along a rainfall gradient in Hawaii: Acacia koa stand structure,
productivity, foliar nutrients, and water- and nutrient-use efficiencies.
Oecologia 102, 277–284. doi:10.1007/BF00329794
Hoły
nska M, Stoch F (2012) Mesocyclops (Crustacea, Copepoda,
Cyclopidae) in the South Pacific islands. Zoologischer Anzeiger 251,
237–252. doi:10.1016/j.jcz.2011.09.004
Hope G, Kershaw AP, van der Kaars S, Xiangjun S, Liew P-M, Heusser LE,
Takahara H, McGlone M, Miyoshi N, Moss PT (2004) History of
vegetation and habitat change in the Austral–Asian region. Quaternary
International 118–119, 103–126. doi:10.1016/S1040-6182(03)00133-2
Käss E, Wink M (1997) Molecular phylogeny and phylogeography of
Lupinus (Leguminosae) inferred from nucleotide sequences of the rbcL
gene and ITS 1+2 regions of rDNA. Plant Systematics and Evolution
208, 139–167. doi:10.1007/BF00985439
Kean J (1991) Aboriginal–Acacia relationships in central Australia. Records
of the South Australian Museum 24, 111–124.
Ladiges PY, Cantrill D (2007) New Caledonia-Australian connections:
comment on biogeographic patterns and geology. Australian
Systematic Botany 20, 383–389. doi:10.1071/SB07018
Ladiges PY, Udovicic F, Nelson G (2003) Australian biogeographical
connections and the phylogeny of large genera in the plant family
Myrtaceae. Journal of Biogeography 30, 989–998.
doi:10.1046/j.1365-2699.2003.00881.x
Larson G (2007) Phylogeny and ancient DNA of Sus provides insights into
Neolithic expansion in inland Southeast Asia and Oceania. Proceedings
of the National Academy of Sciences of the United States of America 104,
4834–4839. doi:10.1073/pnas.0607753104
Lewis GP, Schrire B, Mackinder B, Lock M (2005) ‘Legumes of the World.’
(Royal Botanic Gardens, Kew: London)
Macphail MK, Hill RS (2001) Fossil record of Acacia in Australia: Eocene to
Recent. In ‘Flora of Australia. Vol. 11A’. (Eds AE Orchard, AJG Wilson)
pp. 13–29. (ABRS/CSIRO Publishing: Melbourne)
Maslin BR (2001a) Introduction to Acacia.In‘Flora of Australia. Vol. 11A’.
(Eds AE Orchard, AJG Wilson) pp. 3–13. (ABRS/CSIRO Publishing:
Melbourne)
Maslin BR (2001b)‘Flora of Australia. Vol. 11B.’(ABRS/CSIRO
Publishing: Melbourne)
Maslin BR (2004) Classification and phylogeny of Acacia. In ‘Evolution of
Ecological and Behavioural Diversity: Australian Acacia Thrips as Model
Organisms’. (Eds BJ Crespi, DC Morris, LA Mound) pp. 97–112. (ABRS/
CSIRO Publishing: Melbourne)
Maslin BR (2008) Generic and subgeneric names in Acacia following
retypification of the genus. Muelleria 26,7–9.
McDonald MW, Maslin BR (2000) Taxonomic revision of the salwoods:
Acacia aulacocarpa Cunn. ex Benth. and its allies (Leguminosae:
Mimosoideae: section Juliflorae). Australian Systematic Botany 13,
21–78. doi:10.1071/SB98031
McDonald MW, Maslin BR, Butcher PA (2001) Utilisation of acacias. In
‘Flora of Australia. Vol. 11A’. (Eds AE Orchard, AJG Wilson) pp. 30–40.
(ABRS/CSIRO Publishing: Melbourne)
Miller JT, Andrew R, Bayer R (2003) Molecular phylogenetics of the
Australian acacias of subg. Phyllodineae (Fabaceae: Mimosoideae)
based on the trnK intron. Australian Journal of Botany 51, 167–177.
doi:10.1071/BT01099
Miller JT, Murphy DJ, Brown GK, Richardson DM, González-Orozco CE
(2011) The evolution and phylogenetic placement of invasive Australian
Acacia species. Diversity & Distributions 17, 848–860.
doi:10.1111/j.1472-4642.2011.00780.x
Moran GF, Muona O, Bell JC (1989a)Acacia mangium: a tropical forest tree
of low genetic diversity. Evolution 43, 231–235. doi:10.2307/2409180
Moran GF, Muona O, Bell JC (1989b) Breeding systems and genetic diversity
in Acacia auriculiformis and A. crassicarpa. Biotropica 21, 250–256.
doi:10.2307/2388652
Murphy DJ, Miller JT, Bayer RJ, Ladiges PY (2003) Molecular phylogeny
of Acacia subgenus Phyllodineae (Mimosoideae: Leguminosae) based on
DNA sequences of the internal transcribed spacer region. Australian
Systematic Botany 16,19–26. doi:10.1071/SB01042
Murphy DJ, Brown GK, Miller JT, Ladiges PY (2010) Molecular phylogeny
of Acacia s.s. (Mimosoideae: Leguminosae) –evidence for major clades
and informal classification. Taxon 59,7–19.
New TR (1984) ‘A Biology of Acacias. (Oxford University Press: Melbourne)
Pearson HL, Vitousek PM (2001) Stand dynamics, nitrogen accumulation,
and symbiotic nitrogen fixation in regenerating stands of Acacia koa.
Ecological Applications 11, 1381–1394.
doi:10.1890/1051-0761(2001)011[1381:SDNAAS]2.0.CO;2
Pedley L (1975) Revision of the extra-Australian species of Acacia subg.
Heterophyllum. Contributions from the Queensland Herbarium 18,
1–24.
Pedley L (1978) A revision of Acacia Mill. in Queensland. Austrobaileya 1,
75–234.
Pedley L (1990) New combinations in Acacia Miller (Leguminosae:
Mimosoideae). Austrobaileya 3, 215–216.
Regueiro M, Mirabal S, Lacau H, Caerio JL, Garcia-Bertrand RL, Herrera RJ
(2008) Austronesian genetic signature in East African Madagascar and
Polynesia. Journal of Human Genetics 53, 106–120.
doi:10.1007/s10038-007-0224-4
Rock JF (1913) ‘The Indigenous Trees of the Hawaiian Islands.’pp. 22–35.
(E. Herrick Brown: Honolulu, HI)
Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic
inference under mixed models. Bioinformatics 19, 1572–1574.
doi:10.1093/bioinformatics/btg180
Soares P, Trejaut JA, Loo J-H, Hill C, Mormina M, Lee C-L, Chen Y-M,
Hudjashov G, Forster P, Macauley V, Bulbeck D, Oppenheimer S, Lin M,
Richards MB (2008) Climate change and postglacial human dispersals in
Southeast Asia. Molecular Biology and Evolution 25, 1209–1218.
doi:10.1093/molbev/msn068
Sun Y (1994) Phylogenetic analysis of Sorghum and related taxa using internal
transcribed spacers of nuclear ribosomal DNA. Theoretical and Applied
Genetics 89,26–32. doi:10.1007/BF00226978
Swofford DL (2002) ‘PAUP*: Phylogenetic Analysis using Parsimony (*and
Other Methods) (version 4.0b.10).’(Sinauer: Sunderland, MA)
Trejaut JA, Kivisild TJ, Loo H, Lee CL, He CL, Hsu CJ, Lee ZY, Lin M (2005)
Traces of archaic mitochondrial lineages persist in austronesian-speaking
Formosan populations. PLoS Biology 3, 1362–1372.
Turnbull JW (1984) Six phyllodinous Acacia species for planting in the
humid tropical Lowlands. Pesquisa Agropecuaria Brasileira 19,69–73.
402 Australian Systematic Botany G. K. Brown et al.
Turnbull JW, Crompton HR, Pinyopusarerk K (Eds) (1998) Recent
developments in acacia planting. ACIAR Proceedings number 82,
27–30 October 1997, Hanoi, Vietnam. (Australian Centre for
International Agriculture Research: Canberra)
van Welzen PC, Turner H, Hovenkamp P (2003) Historical biogeography
of Southeast Asia and the West Pacific, or the generality of unrooted
networks as historical biogeographic hypotheses. Journal of
Biogeography 30, 181–192. doi:10.1046/j.1365-2699.2003.00827.x
Vassal J (1969) A propos des Acacia heterophylla et koa. Bulletin de la
Société D’Histoire Naturelle de Toulouse 105, 443–447.
Wagner WL, Herbst DR, Sohmer SH (1990) ‘Manual of the Flowering Plants
of Hawaii.’(University of Hawaii Press and Bishop Museum Press:
Honolulu, HI)
Whitesell CD (1964) Silvical characteristics of koa (Acacia koa Gray).
USDA Forest Service, Pacific Southwest Forest and Range Experiment
Station, Research Paper PSW-16, pp. 1–11. (Berkley, CA)
Yu H (2007) Physiological comparisons of true leaves and phyllodes in
Acacia mangium seedlings. Photosynthetica 45, 312–316.
doi:10.1007/s11099-007-0053-x
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