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Historical biogeography of Melicope (Rutaceae) and its close relatives with a special emphasis on Pacific dispersals: Pacific Biogeography of Melicope (Rutaceae)

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Historical biogeography of Melicope (Rutaceae) and its close relatives with a special emphasis on Pacific dispersals: Pacific Biogeography of Melicope (Rutaceae)

Abstract and Figures

The genus Melicope (Rutaceae) occurs on most Pacific archipelagos and is perfectly suited to study Pacific biogeography. The main goal was to infer the age, geographic origin and colonization patterns of Melicope and its relatives. We sequenced three nuclear and two plastid markers for 332 specimens that represent 164 species in 16 genera of Rutaceae. Phylogenetic reconstruction, molecular dating, ancestral area reconstruction and diversification analyses were carried out. The two main clades (Acronychia- Melicope and Euodia) originated in Australasia and their crown ages are dated to the Miocene. Diversification rates differed among the subclades and were lowest in the Euodia lineage and highest in the Hawaiian Melicope lineage. The Malagasy and Mascarene species form a clade, which split from its SE Asian relatives in the Pliocene/Pleistocene. At least eight colonizations to the Pacific islands occurred. The timing of all colonizations except for the Hawaiian group is congruent with age of the island ages. Australia, New Guinea and New Caledonia have been the source of colonizations into the Pacific islands in the Melicope clade. Melicope shows high dispersability and has colonized remote archipelagos such as the Austral and Marquesas Islands each twice. Colonization of islands of the Hawaiian-Emperor seamount chain likely predates the ages of the current main islands, and the initial colonization to Kaua'i occurred after the splitting of the Hawaiian lineage into two subclades. Wider ecological niches and adaptations to bird-dispersal likely account for the much higher species richness in the Acronychia- Melicope clade compared to the Euodia clade.
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Research Article
doi: 10.1111/jse.12299
Historical biogeography of Melicope (Rutaceae) and its
close relatives with a special emphasis on Pacic dispersals
Marc S. Appelhans
1,2
*, Jun Wen
2
, Marco Duretto
3
, Darren Crayn
4
, and Warren L. Wagner
2
1
Department of Systematics, Biodiversity and Evolution of Plants, Albrecht-von-Haller Institute of Plant Sciences, University of Goettingen,
Untere Karspuele 2, 37073 Goettingen, Germany
2
Department of Botany, National Museum of Natural History, Smithsonian Institution, PO Box 37012, Washington, DC 20013-7012, USA
3
National Herbarium of New South Wales, Royal Botanic Gardens & Domain Trust, Mrs Macquaries Rd, Sydney NSW 2000, Australia
4
Australian Tropical Herbarium, James Cook University, PO Box 6811, Cairns QLD 4870, Australia
*Author for correspondence. E-mail: marc.appelhans@biologie.uni-goettingen.de
Received 17 October 2017; Accepted 22 December 2017; Article first published online xx Month 2018
Abstract The genus Melicope (Rutaceae) occurs on most Pacic archipelagos and is perfectly suited to study
Pacic biogeography. The main goal was to infer the age, geographic origin and colonization patterns of Melicope
and its relatives. We sequenced three nuclear and two plastid markers for 332 specimens that represent 164 species
in 16 genera of Rutaceae. Phylogenetic reconstruction, molecular dating, ancestral area reconstruction and
diversication analyses were carried out. The two main clades (Acronychia-Melicope and Euodia) originated in
Australasia and their crown ages are dated to the Miocene. Diversication rates differed among the subclades and
were lowest in the Euodia lineage and highest in the Hawaiian Melicope lineage. The Malagasy and Mascarene
species form a clade, which split from its SE Asian relatives in the Pliocene/Pleistocene. At least eight colonizations
to the Pacic islands occurred. The timing of all colonizations except for the Hawaiian group is congruent with age of
the island ages. Australia, New Guinea and New Caledonia have been the source of colonizations into the Pacic
islands in the Melicope clade. Melicope shows high dispersability and has colonized remote archipelagos such as the
Austral and Marquesas Islands each twice. Colonization of islands of the Hawaiian-Emperor seamount chain likely
predates the ages of the current main islands, and the initial colonization to Kaua’i occurred after the splitting of the
Hawaiian lineage into two subclades. Wider ecological niches and adaptations to bird-dispersal likely account for the
much higher species richness in the Acronychia-Melicope clade compared to the Euodia clade.
Key words: Acronychia, dispersal, Euodia,Melicope, Pacic biogeography, Rutaceae.
1 Introduction
Due to their geographic isolation, mostly recent volcanic
origin and their high endemicity, Pacic archipelagos are
particularly interesting for biogeographic and evolutionary
studies. Most Pacic islands are of volcanic origin and have
never been in direct contact with continental landmasses
(Neall & Trewick, 2008). Pacic islands that consist of
continental crust – e.g., New Caledonia and New Zealand –
have long been separated from other continental landmasses
and elements of their oras and faunas arrived after their
isolation (Sharma & Wheeler, 2013). Colonizers of Pacic
islands most likely arrived by means of long-distance dispersal
(LDD) events (Nathan et al., 2008). Different vectors
facilitating LDD have been identied; the most common
being birds, wind, ocean currents, and driftwood rafts (Donlan
& Nelson, 2003; Cowie & Holland, 2006; Wenny et al., 2016). A
‘standard vector’ of dispersal has been proposed for many
species based on morphological characters (Carlquist, 1967).
However the relationship between morphology and dispersal
is difcult to quantify and it has been proposed that multiple
or non-standard vectors might account for LDD events
(Higgins et al., 2003; Nathan et al., 2008). Molecular
phylogenetic studies have identied examples of single LDD
events across thousands of kilometers (Le Roux et al., 2014),
as well as shorter distance events as stepping-stone dispersals
(Harbaugh et al., 2009). Since only a small percentage of
the Pacic region consists of exposed land, successful
colonizations, especially of the more remote islands, can be
considered to be extremely rare. Many lineages once thought
to represent independent colonizations on a particular
archipelago have been shown to be the result of an extensive
radiation after a single colonization event. The most notable
example being the Hawaiian Lobeliads (Campanulaceae),
the largest island radiation of angiosperms (Givnish et al.,
2009). Pacic lineages are mostly of Asian, Australasian or
American origin and only a few examples of an African origin
are known (Baldwin & Wagner, 2010; Keeley & Funk, 2011).
Melicope J.R.Forst. & G.Forst. (Rutaceae; Citrus family) and
its close relatives (hereinafter the Acronychia-Euodia-Melicope
group) occur on most Pacic archipelagos and the group is
therefore perfectly suited to study Pacic biogeography and
JSE Journal of Systematics
and Evolution
XXX 2018 | Volume 9999 | Issue 9999 | 1–24 © 2018 Institute of Botany, Chinese Academy of Sciences
dispersal routes. Recent phylogenetic studies have demon-
strated that Melicope is not monophyletic and several genera
need to be merged into it or into Acronychia J.R.Forst. &
G.Forst. and Euodia J.R.Forst. & G.Forst. to ensure monophyly
of each genus (Appelhans et al., 2014a, 2014b; Holzmeyer
et al., 2015). Melicope (240 spp.) is the largest genus in
Rutaceae and occurs in Madagascar and the Mascarene
Islands, throughout SE Asia, Malesia, Australasia, and on most
Pacic archipelagos. Its centers of species richness and
endemicity are the Hawaiian Islands and New Guinea (Hartley,
2001). Acronychia (49 spp.) is the second largest genus of the
Acronychia-Euodia-Melicope group and is mainly conned to
eastern Australia and New Guinea with two species extending
west to Java and India, and two eastward to the Solomon
Islands and New Caledonia (Hartley, 1974, 2013; Holzmeyer
et al., 2015). Euodia (7 spp.) is more restricted and is present in
eastern Australia, New Guinea and the South Pacic from New
Britain and New Caledonia to Samoa and Niue (Hartley, 2001).
The Acronychia-Euodia-Melicope group consists of 15
genera and about 360 species (Kubitzki et al., 2011; Appelhans
et al., 2014a). Of these, Comptonella Baker f., Dutaillyea Baill.,
Picrella Baill. (all New Caledonia), Platydesma H.Mann
(Hawaii) and Sarcomelicope Engl. (Australia to Fiji) are nested
within Melicope while Maclurodendron T.G.Hartley (Malay
Peninsula to the Philippines and Hainan) is nested within
Acronychia.Platydesma has recently been merged into
Melicope (Appelhans et al., 2017). Medicosma Hook.f (New
Guinea, E Australia, New Caledonia) and Tetractomia Hook.f
(Malay Peninsula to the Solomon Islands) are consecutive
sister groups of the Acronychia-Melicope clade. Brombya F.
Muell. (Australia), Pitaviaster T.G.Hartley (Australia), along
with Melicope vitiora (F.Muell.) T.G.Hartley, group with
Euodia, and this clade is sister to Perryodendron T.G.Hartley
(Moluccas to New Britain) (Appelhans et al., 2014a). The
monotypic Dutailliopsis T.G.Hartley (New Caledonia) is a
potential member of the Melicope clade based on morpho-
logical characters (Hartley, 1997, 2001; Bayly et al., 2013), but
it has not been sampled in any molecular phylogenetic study.
Unpublished results (M. Duretto) indicate Zieria Sm.
(Australia & New Caledonia), Neobyrnesia J.A.Armstr. and
Boronia Sm. section Cyanothamnus (Lindl.) F.Muell.
(Australia) classify within the Acronychia-Euodia-Melicope
group but are separated from other genera by long branches.
These last three taxa are not included in this analysis. Even
though the Acronychia-Melicope clade and the Euodia clade
occupy similar habitats, they differ largely in terms of
distributional range and species richness.
The main goal of this study is to establish a dated molecular
phylogeny with an ancestral area reconstruction and a
diversication analysis of the Acronychia-Euodia-Melicope
group to (1) infer the geographic origin and the temporal
diversication history of the group; (2) reconstruct major
dispersal routes in the Pacic region; and (3) evaluate if there
are different diversication rates among subclades.
2 Material and Methods
2.1 Taxon sampling & datasets
The taxon sampling of this study was largely based on that
of Appelhans et al. (2014a, 2014b) and Holzmeyer et al.
(2015) with several additional species mainly from Pacic
archipelagos sampled. A total number of 332 specimens,
representing 164 species and 16 genera, were included in this
study (Table 1): Melicope (118 out of 235 species and 12
unidentied specimens), Acronychia (24/48), Brombya (1/2),
Comptonella (4/8), Dutaillyea (1/2), Euodia (4/6), Macluroden-
dron (1/6), Medicosma (1/25), Perryodendron (1/1), Picrella (2/3),
Pitaviaster (1/1), Sarcomelicope (1/9), Tetractomia (1/6). Dutail-
liopsis,Boronia section Cyanothamnus,Neobyrnesia and Zieria
were the only putative relatives that were not sampled. We
sampled throughout the distributional range of Melicope and
its relatives with particularly comprehensive sampling of the
Pacic species (72/111). One specimen of Boronia (section
Boronella (Baill.) Duretto & Bayly) and three specimens of
Myrtopsis O.Hoffm. were included as outgroups based on
previous phylogenetic studies (Bayly et al., 2013; Appelhans
et al., 2014a).
For the ancestral area reconstructions (AAR) and diversi-
cation analyses, a reduced dataset containing only a single
specimen for each species was used. For species found to be
polyphyletic, one specimen for each evolutionary lineage was
included. This dataset contains 166 species/specimens (Table 1,
specimens in bold type).
2.2 Molecular lab work and phylogenetic analyses
Our datasets included nuclear markers ETS, ITS and NIAi3 and
plastid markers psbA-trnH and trnL-trnF. DNA extraction, PCR
amplication, contig assembly, construction of alignments
and model selection followed Appelhans et al. (2014b). All
sequences were deposited at EMBL/Genbank (Table 1).
Alignment was straightforward except for the psbA-trnH
region which contained many, often large (ca. 100 bp) indels.
After excluding bases that could not be aligned with
condence, the psbA-trnH alignment was reduced from 1101
to 509 bp. Phylogenetic reconstructions were conducted with
mrbayes 3.2.5 (Ronquist et al., 2012) using the best-t models
of sequence evolution for each marker (Table 2) and applying
the settings described by Appelhans et al. (2014b). We
checked if effective sample sizes (ESS) were above 200 for all
parameters using Tracer 1.6.0 (Rambaut et al., 2014) and
discarded 10% of the trees as burnin before calculating a 50%
majority rule consensus tree in MrBayes. Clades with posterior
probabilities (pp) of 0.95 were considered statistically
supported.
2.3 Molecular dating analyses
Molecular dating analyses were performed using BEAST
v.1.8.4 (Drummond et al., 2012). The dated maximum clade
credibility consensus tree from the reduced dataset was used
in the downstream analyses (AAR, diversication analyses).
While Rutaceae have a good fossil record (Appelhans et al.,
2012), no fossils suitable for molecular dating are known for
the Acronychia-Euodia-Melicope clade. The oldest fossils
possibly belonging to this clade are from the Miocene-
Oligocene boundary in Australia and New Zealand (“aff.
Acronychia, aff. Euodia” [Blackburn & Sluiter, 1994] and “?
Melicope” [Conran et al., 2014]) but since they are of uncertain
afnity they were not considered further. Other Melicope
(sub)fossils (Burney et al., 2001; Kershaw et al., 2007) were not
suited because of their young age (Late Pleistocene or
Holocene). Fossils formerly assigned to Euodia (Tiffney, 1980,
2 Appelhans et al.
J. Syst. Evol. 9999 (9999): 1–24, 2018 www.jse.ac.cn
Table 1 Voucher information, area codes for biogeographic analyses and Genbank numbers of all individuals used in this study
Taxon Voucher information Area
code
trnL-trnF ITS ETS psbA-trnH NIAi3
Collector & number (Herbarium) Origin
A. acronychioides Forster PIF30987 (L) Australia, Queensland D LN849177 LN849136 LN849220
A. acuminata Ford 3997 (CNS) Australia, Queensland D LN849178 LN849137 LN849221 LN849160 LN849199
A. baeuerlenii Beesley 1080a (NSW) Australia, NSW D LN849179 LN849138 LN849222 LN849161 LN849200
A. baeuerlenii Rossetto ABNIG1 (NSW) Australia, NSW D LN849180 LN849139 LN849223 LN849162 LN849201
A. brassii Appelhans 454 (LAE, US) Papua New Guinea D HG971153 HG971304 HG971458 HG971025 HG971612
A. brassii Appelhans 466 (LAE, US) Papua New Guinea D HG971154 HG971305 HG971459 HG971026 HG971613
A. brassii Appelhans 467 (LAE, US) Papua New Guinea D HG971155 HG971306 HG971460 HG971027 HG971614
A. cartilaginea Takeuchi 23857 (A) Papua New Guinea D LN849140 LN849224
A. chooreechillum Telford 11393 (NSW) Australia, Queensland D LN849181 LN849141 LN849226 LN849163 LN849202
A. eungellensis Forster PIF25513 (CNS) Australia, Queensland D LN849228 LN849164 LN849203
A. imperforata Forster PIF30952 (L) Australia, Queensland D LN849182 LN849143 LN849231 LN849204
A. laevis Forster PIF30953 (L) Australia, Queensland D LN849183 LN849144 LN849232
A. ledermannii Appelhans 426 (LAE, US) Papua New Guinea D HG971156 HG971307 HG971461 HG971028 HG971615
A. ledermannii Appelhans 448 (LAE, US) Papua New Guinea D HG971157 HG971308 HG971462 HG971029 HG971616
A. ledermannii Appelhans 458 (LAE, US) Papua New Guinea D HG971158 HG971309 HG971463 HG971030 HG971617
A. littoralis Rossetto ALBAL1 (NSW) Australia, NSW D AY588597 LN849233 LN849165 LN849205
A. littoralis Rossetto ALAB1 (NSW) Australia, NSW D LN849184 LN849234 LN849166 LN849207
A. littoralis Rossetto ALSC2 (NSW) Australia, NSW D LN849185 LN849235 LN849167 LN849206
A. murina Utteridge 542 (A) Papua New Guinea D LN849186 LN849145 LN849236
A. murina Regalado 1023 (A) Papua New Guinea D LN849187 LN849146 LN849237 LN849168 LN849209
A. murina Takeuchi 24793 (A) Papua New Guinea D LN849188 LN849147 LN849238 LN849208
A. oblongifolia Winsbury 97 (CBG) Australia, NSW D EU493242 EU493185 HG971464 EU493204
A. octandra Forster PIF34176 (MEL) Australia, Queensland D LN849190 LN849149 LN849240 LN849170
A. parviflora Ford 4434 (CNS) Australia, Queensland D LN849191 LN849150 LN849241 LN849211
A. pauciflora Rossetto APAWIL1 (NSW) Australia, NSW D LN849192 LN849151 LN849242 LN849171 LN849212
A. pedunculata de Wilde 6834 (L) Thailand B, C, D HG002754 HG002398 HG002527 HG002652 HG002957
A. pedunculata Brambach 1503 (GOET) Indonesia, Sulawesi B, C, D LN849193 LN849152 LN849243 LN849214
A. pedunculata Wen 12364 (US) Indonesia, Java B, C, D LN849153 LN849244 LN849172 LN849213
A. pubescens Rossetto APUWIL1 (NSW) Australia, NSW D LN849194 LN849154 LN849173 LN849215
A. pullei Appelhans 460 (US) Papua New Guinea D HG971159 HG971310 HG971465 HG971031 HG971618
A. reticulata Coode 8081 (L) Indonesia, Papua D HG971160 HG971311 HG971466
A. suberosa Forster PIF28797 (L) Australia, Queensland D LN849195 LN849155 LN849246
A. suberosa Rossetto ASNIG1 (NSW) Australia, NSW D LN849196 LN849156 LN849247 LN849174 LN849216
A. trifoliolata var.
microcarpa
James 459 (LAE, BISH, GOET) Papua New Guinea C, D HG971161 HG971312 HG971467 HG971032 HG971619
A. trifoliolata var.
microcarpa
Appelhans 416 (LAE, US) Papua New Guinea C, D HG971162 HG971313 HG971468 HG971033 HG971620
Continued
Pacific biogeography of Melicope (Rutaceae) 3
www.jse.ac.cn J. Syst. Evol. 9999 (9999): 1–24, 2018
Table 1 Continued
Taxon Voucher information Area
code
trnL-trnF ITS ETS psbA-trnH NIAi3
Collector & number (Herbarium) Origin
A. vestita Forster PIF27548 (L) Australia, Queensland D LN849157 LN849248 LN849217
A. wilcoxiana Rossetto AWIL1 (NSW) Australia, NSW D LN849197 LN849158 LN849249 LN849175 LN849218
Bo. spec. Lowry 6481 (MO) New Caledonia D HG971285 HG971314 HG971469 HG971621
Br. platynema Ford 4819 (L) Australia D HG971163 HG971315 HG971034 HG971622
C. baudouinii MacKee 29450 (L) New Caledonia D HG971165 HG971317 HG971471
C. microcarpa Munzinger 679 (MO) New Caledonia D HG971274 þ
HG971286
HG971318 HG971472 HG971035 HG971623
C. microcarpa Lowry 5734 (MO) New Caledonia D HG971275 þ
HG971287
HG971319 HG971473 HG971036 HG971624
C. oreophila McPherson 18544 (MO) New Caledonia D HG971166 HG971320 HG971474 HG971037 HG971625
C. sessilifoliola McPherson 18023 (MO) New Caledonia D HG971276 þ
HG971288
HG971322 HG971475 HG971038 HG971626
C. sessilifoliola Van Balgooy 7053 (L) New Caledonia D HG971167 HG971323 HG971476 HG971039
D. spec. Munzinger 790 (MO) New Caledonia D HG971277 HG971324 HG971477 HG971040 HG971627
E. hortensis Appelhans 398 (US) Singapore Botanical Garden
(2007 0570C)
D, F HG971168 HG971325 HG971478 HG971041 HG971628
E. hortensis Drake 235 (US) Polynesia, Tonga D, F HG002786 þ
HG002862
HG002399 HG002528 HG002653 HG002958
E. hylandii Forster 25754 (L) Australia, Queensland D HG971169 HG971326 HG971479 HG971042 HG971629
E. montana James 381 (LAE, BISH, GOET) Papua New Guinea D HG971170 HG971327 HG971480 HG971043 HG971630
E. pubifolia Sankowsky 1711 (QRS) Australia D EU493243 EU493186 HG971481 EU493205 HG971631
M. accedens Beaman 7360 (L) Borneo B, C HG971173 HG971331 HG971485 HG971046 HG971632
M. accedens Wen 10990 (US) Vietnam B, C HG971174 HG971332 HG971486 HG971047 HG971633
M. accedens Kato 20120218182 (MAK) Malaysia B, C AB766301 AB766300 AB766303
M. adscendens Oppenheimer 40001 (US) USA, Hawaii, Maui G HG002787 þ
HG002863
HG002400 HG002529 HG002654 HG002959
M. adscendens Oppenheimer 40002 (US) USA, Hawaii, Maui G HG002788 þ
HG002864
HG002401 HG002530 HG002655 HG002960
M. adscendens Wood 7672 (PTBG) USA, Hawaii, Maui G HG002789 þ
HG002865
HG002402 HG002531 HG002656 HG002961
M. albiflora Whistler 2004 (B) Samoa F MG668986 MG595154 MG668941 – MG668968
M. aneura Appelhans 418 (LAE, US) Papua New Guinea D HG971175 HG971333 HG971487 HG971048 HG971634
M. aneura Appelhans 439 (LAE, US) Papua New Guinea D HG971176 HG971334 HG971488 HG971049 HG971635
M. aneura Appelhans 441 (LAE, US) Papua New Guinea D HG971177 HG971335 HG971489 HG971050 HG971636
M. anisata Wagner 6892 (US) USA, Hawaii, Kaua‘i G HG002790 þ
HG002866
HG002403 HG002532 HG002657 HG002962
Continued
4 Appelhans et al.
J. Syst. Evol. 9999 (9999): 1–24, 2018 www.jse.ac.cn
Table 1 Continued
Taxon Voucher information Area
code
trnL-trnF ITS ETS psbA-trnH NIAi3
Collector & number (Herbarium) Origin
M. anisata Wood 5844 (PTBG) USA, Hawaii, Kaua‘i G HG002791 þ
HG002867
HG002404 HG002533 HG002658 HG002963
M. anomala Uttridge 359 (L) Indonesia, Papua D HG971178 HG971336 HG971490 HG971051 HG971637
M. balgooyi Wood 9698 (BISH, NY) Austral Islands F HG971246 HG971418 HG971571 HG971117 HG971710
M. balgooyi Wood 9727 (BISH, NY) Austral Islands F HG971247 HG971419 HG971572 HG971118 HG971711
M. balloui Wood 7685 (PTBG) USA, Hawaii, Maui G HG002792 þ
HG002868
HG002405 HG002534 HG002659 HG002964
M. barbigera Wagner 6896 (US) USA, Hawaii, Kaua‘i G HG002793 þ
HG002869
HG002406 HG002535 HG002660 HG002965
M. bonwickii Wen 10286 (US) Indonesia, Sulawesi C, D HG971179 HG971337 HG971491 HG971052 HG971638
M. borbonica Adersen 5564 (C) La R
eunion A HG971180 HG971338 HG971492 HG971053
M. brassii (cf) Appelhans 436 (LAE, US) Papua New Guinea D HG971181 HG971339 HG971493 HG971054 HG971639
M. broadbentiana Telford 9474 (CANB) Australia, Queensland D HG971278 þ
HG971290
HG971340 HG971494
M. broadbentiana Gray 435 (L) Australia, Queensland D HG971341 HG971495 HG971055
M. capillacea Smith 4992 (NY) Fiji F HG971291 HG971342 HG971640
M. christophersenii Wood 7894 (PTBG) USA, Hawaii, O‘ahu G HG002794 þ
HG002870
HG002407 HG002536 HG971641
M. clemensiae Pearce 96017 (L) Borneo C HG971292 HG971343 HG971496
M. clusiifolia Wagner 6894 (US) USA, Hawaii, Kaua‘i G HG002755 HG002408 HG002537 HG002966
M. clusiifolia Wagner 6900 (PTBG) USA, Hawaii, O‘ahu G EU493235 EU493178 HG002538 EU493197 HG002967
M. clusiifolia Wagner 6908 (US) USA, Hawaii, O‘ahu G HG002795 þ
HG002871
HG002409 HG002539 HG002968
M. clusiifolia Wagner 6912 (US) USA, Hawaii, Maui G HG002796 þ
HG002872
HG002410 HG002540 HG002661 HG002969
M. clusiifolia Wood 12406 (PTBG) USA, Hawaii, Hawai‘i G HG002797 þ
HG002873
HG002411 HG002541 HG002662 HG002970
M. clusiifolia Wood 8151 (PTBG) USA, Hawaii, Kaua‘i G HG002798 þ
HG002874
HG002412 HG002542 HG002663 HG002971
M. clusiifolia Wood 8253 (PTBG) USA, Hawaii, Kaua‘i G HG002799 þ
HG002875
HG002413 HG002543 HG002972
M. coodeana Larsen 52 (C) La R
eunion A HG971182 HG971345 HG971498 HG971057 HG971642
M. cornuta Wood 2776 (PTBG) USA, Hawaii, O‘ahu G HG002936 HG002504 HG002644
M. crassifolia Soejarto 8054 (L) Philippines C HG971452 HG971610
M. cravenii Regaldo 1027 (NY) Papua New Guinea D HG971293 HG971346 HG971499 HG971643
M. cravenii Appelhans 432 (LAE, US) Papua New Guinea D HG971183 HG971347 HG971500 HG971058 HG971644
Continued
Pacific biogeography of Melicope (Rutaceae) 5
www.jse.ac.cn J. Syst. Evol. 9999 (9999): 1–24, 2018
Table 1 Continued
Taxon Voucher information Area
code
trnL-trnF ITS ETS psbA-trnH NIAi3
Collector & number (Herbarium) Origin
M. cruciata Wood 13777 (PTBG) USA, Hawaii, Kaua‘i G HG002800 þ
HG002876
HG002414 HG002544 HG002664 HG002973
M. cruciata Wood 8146 (PTBG) USA, Hawaii, Kaua‘i G HG002801 þ
HG002877
HG002415 HG002545 HG002665 HG002974
M. cruciata Wood 8188 (PTBG) USA, Hawaii, Kaua‘i G HG002802 þ
HG002878
HG002416 HG002546 HG002666 HG002975
M. cucullata Kuruvoli 16067 (NY) Fiji D, F HG971294 HG971348 HG971645
M. degeneri Wood 12137 (PTBG) USA, Hawaii, Kaua‘i G HG002803 þ
HG002879
HG002417 HG002547 HG002667 HG002976
M. degeneri Wood 7442 (PTBG) USA, Hawaii, Kaua‘i G HG002756 HG002418 HG002548 HG002668 HG002977
M. degeneri Wood 7445 (PTBG) USA, Hawaii, Kaua‘i G EU493236 EU493179 HG002549 EU493198 HG002978
M. degeneri Wood 7662 (PTBG) USA, Hawaii, Kaua‘i G HG002757 HG002419 HG002550 HG002669 HG002979
M. denhamii Appelhans 486 (GOET) cultivated Hortus Botanicus
Leiden
C, D, E,
F
HG971184 HG971349 HG971501 HG971059 HG971646
M. denhamii Takeuchi 16796 (L) Papua New Guinea C, D, E,
F
HG971185 HG971350 HG971502 HG971060 HG971647
M. denhamii Utteridge 266 (L) Papua New Guinea C, D, E,
F
HG971186 HG971351 HG971503 HG971061 HG971648
M. denhamii Appelhans 401 (LAE, US) Papua New Guinea C, D, E,
F
HG971187 HG971352 HG971504 HG971062 HG971649
M. denhamii Appelhans 402 (LAE, US) Papua New Guinea C, D, E,
F
HG971188 HG971353 HG971505 HG971063 HG971650
M. denhamii Appelhans 419 (LAE, US) Papua New Guinea C, D, E,
F
HG971189 HG971354 HG971506 HG971064 HG971651
M. denhamii Appelhans 428 (LAE, US) Papua New Guinea C, D, E,
F
HG971190 HG971355 HG971507 HG971652
M. denhamii Appelhans 453 (LAE, US) Papua New Guinea C, D, E,
F
HG971191 HG971356 HG971508 HG971065 HG971653
M. denhamii Appelhans 464 (LAE, US) Papua New Guinea C, D, E,
F
HG971192 HG971357 HG971509 HG971066 HG971654
M. denhamii Appelhans 468 (LAE, US) Papua New Guinea C, D, E,
F
HG971193 HG971358 HG971510 HG971655
M. denhamii Appelhans 396 (US) cultivated SING (Nr.
20100535A)
C, D, E,
F
HG971194 HG971359 HG971511 HG971067 HG971656
M. durifolia Appelhans 424 (US) Papua New Guinea D HG971195 HG971360 HG971512 HG971068 HG971657
M. durifolia Appelhans 455 (LAE, US) Papua New Guinea D HG971196 HG971361 HG971513 HG971069 HG971658
M. durifolia Appelhans 465 (LAE, US) Papua New Guinea D HG971197 HG971362 HG971514 HG971070 HG971659
Continued
6 Appelhans et al.
J. Syst. Evol. 9999 (9999): 1–24, 2018 www.jse.ac.cn
Table 1 Continued
Taxon Voucher information Area
code
trnL-trnF ITS ETS psbA-trnH NIAi3
Collector & number (Herbarium) Origin
M. elleryana Lorence 6602 (PTBG) cultivated NTBG D EU493241 EU493184 HG002551 EU493203 HG002980
M. elleryana Weiblen WS4C-0692 (MIN) Papua New Guinea D HG971198 HG971363 HG971515 HG971071 HG971660
M. elleryana Weiblen WS5C-0774 (MIN) Papua New Guinea D HG971199 HG971364 HG971516 HG971072 HG971661
M. elleryana Appelhans 403 (LAE, US) Papua New Guinea D HG971200 HG971365 HG971517 HG971073 HG971662
M. elleryana Appelhans 404 (LAE, US) Papua New Guinea D HG971201 HG971366 HG971518 HG971074 HG971663
M. elleryana Appelhans 405 (LAE, US) Papua New Guinea D HG971202 HG971367 HG971519 HG971075 HG971664
M. elleryana Appelhans 406 (LAE, US) Papua New Guinea D HG971203 HG971368 HG971520 HG971076 HG971665
M. elleryana Appelhans 407 (LAE, US) Papua New Guinea D HG971204 HG971369 HG971521 HG971077 HG971666
M. elleryana Appelhans 411 (LAE, US) Papua New Guinea D HG971205 HG971370 HG971522 HG971078 HG971667
M. elleryana Appelhans 412 (LAE, US) Papua New Guinea D HG971206 HG971371 HG971523 HG971079 HG971668
M. elleryana Appelhans 413 (LAE, US) Papua New Guinea D HG971207 HG971372 HG971524 HG971080 HG971669
M. elleryana Appelhans 414 (US) Papua New Guinea D HG971208 HG971373 HG971525 HG971081 HG971670
M. elleryana Appelhans 395 (LAE, US) cultivated SING (Nr.
20103854A)
D HG971209 HG971374 HG971526 HG971082 HG971671
M. elliptica Wagner 6906 (US) USA, Hawaii, O‘ahu G HG002758 HG002420 HG002552 HG002670 HG002981
M. elliptica Wagner 6907 (US) USA, Hawaii, O‘ahu G HG002804 þ
HG002880
HG002421 HG002553 HG002671 HG002982
M. feddei Perlman 16139 (PTBG) USA, Hawaii, Kaua‘i G HG002805 þ
HG002881
HG002422 HG002554 HG002672 HG002983
M. feddei Wood 7514 (PTBG) USA, Hawaii, Kaua‘i G HG002806 þ
HG002882
HG002423 HG002555 HG002673 HG002984
M. feddei Wood 8263 (PTBG) USA, Hawaii, Kaua‘i G HG002807 þ
HG002883
HG002424 HG002556 HG002674 HG002985
M. forbesii Curry 1616 (L) Vanuatu D HG971210 HG971375 HG971527 HG971083 HG971672
M. frutescens Laman 936 (L) Borneo C, D HG971344 HG971497 HG971056
M. frutescens Brambach 464 (GOET) Indonesia, Sulawesi C, D MG668987 MG595156 MG668943 MG668958 MG668969
M. glabra Ambri AA1575 (L) Indonesia, Borneo B, C MG668988 MG595157 MG668944 MG668959 MG668970
M. glabra Kato 20120215152 (MAK) Malaysia B, C AB766293 AB766292 AB766295
M. glabra Kato 20120215148 (MAK) Malaysia B, C AB766297 AB766296 AB766299
M. glomerata Wen 5856 (US) Vietnam B HG971211 HG971376 HG971528 HG971084 HG971673
M. goilalensis James 494 (LAE, BISH, GOET) Papua New Guinea D HG971295 HG971377 HG971529 HG971085 HG971674
M. grisea 404826 (MAK) Japan, Chichijima Island E AB766345 AB766344 AB766347
M. grisea var.
crassifolia
404821 (MAK) Japan, Chichijima Island E AB766349 AB766348 AB766351
M. grisea var.
crassilfolia
Katok M620 (MAK) Japan, Chichijima Island E AB766353 AB766352 AB766355
Continued
Pacific biogeography of Melicope (Rutaceae) 7
www.jse.ac.cn J. Syst. Evol. 9999 (9999): 1–24, 2018
Table 1 Continued
Taxon Voucher information Area
code
trnL-trnF ITS ETS psbA-trnH NIAi3
Collector & number (Herbarium) Origin
M. haleakalae Oppenheimer 60141 (US) USA, Hawaii, Maui G HG002808 þ
HG002884
HG002425 HG002557 HG002675 HG002986
M. haupuensis Wood 7724 (PTBG, US) USA, Hawaii, Kaua‘i G HG002809 þ
HG002885
HG002426 HG002558 HG002676 HG002987
M. haupuensis Wood 7725 (PTBG) USA, Hawaii, Kaua‘i G HG002810 þ
HG002886
HG002427 HG002559 HG002677 HG002988
M. hawaiensis Oppenheimer 60151 (US) USA, Hawaii, Maui G HG002811 þ
HG002887
HG002428 HG002560 HG002678 HG002989
M. hawaiensis Wood 12102 (PTBG) USA, Hawaii, Maui G HG002812 þ
HG002888
HG002429 HG002561 HG002679 HG002990
M. hivaoaensis Meyer 826 Marquesas Islands F EU493230 EU493173 HG002562 EU493192 HG002991
M. hookeri Riswan 61 (L) Borneo B, C HG971212 HG971378 HG971530
M. hosakae Wagner 6903 (US) USA, Hawaii, O‘ahu G HG002813 þ
HG002889
HG002430 HG002563 HG002680 HG002992
M. inopinata Meyer 887 Marquesas Islands F EU493233 EU493176 HG002564 EU493195 HG002993
M. jonesii Ford 4684 (L) Australia, Queensland D HG971213 HG971379 HG971531 HG971086 HG971675
M. kavaiensis Wood 12270 (PTBG) USA, Hawaii, Kaua‘i G HG002814 þ
HG002890
HG002431 HG002565 HG002681 HG002994
M. kavaiensis Wood 8182 (PTBG) USA, Hawaii, Kaua‘i G HG002759 HG002432 HG002566 HG002682
M. knudsenii Perlman 19411 (PTBG) USA, Hawaii, Kaua‘i G HG002815 þ
HG002891
HG002433 HG002567 HG002683 HG002995
M. knudsenii Wagner 6891 (US) USA, Hawaii, Kaua‘i G EU493225 EU493168 HG002568 EU493187 HG002996
M. knudsenii Wood 12455 (PTBG) USA, Hawaii, Kaua‘i G HG002816 þ
HG002892
HG002434 HG002569 HG002684 HG002997
M. knudsenii Wood 15101 (PTBG) USA, Hawaii, Kaua‘i G HG002760 HG002435 HG002570 HG002685 HG002998
M. knudsenii Wood 7667 (PTBG) USA, Hawaii, Maui G HG002817 þ
HG002893
HG002436 HG002571 HG002686 HG002999
M. knudsenii Wood 7678 (PTBG) USA, Hawaii, Maui G HG002818 þ
HG002894
HG002437 HG002572 HG002687 HG003000
M. knudsenii Wood 7696 (PTBG) USA, Hawaii, Kaua‘i G HG002761 HG002438 HG002573 HG002688 HG003001
M. knudsenii Wood 7697 (PTBG) USA, Hawaii, Kaua‘i G HG002819 þ
HG002895
HG002439 HG002574 HG002689 HG003002
M. lasioneura (cf) Munzinger 939 (P) New Caledonia D HG971296 HG971380 HG971676
M. latifolia Polak 1044 (L) New Guinea C, D HG002820 þ
HG002896
HG002440 HG002575 HG002690 HG003003
M. latifolia Lorence 10298 (PTBG) cultivated NTBG (Nr.
990589)
C, D HG971214 HG971381 HG971532 HG971087 HG971677
Continued
8 Appelhans et al.
J. Syst. Evol. 9999 (9999): 1–24, 2018 www.jse.ac.cn
Table 1 Continued
Taxon Voucher information Area
code
trnL-trnF ITS ETS psbA-trnH NIAi3
Collector & number (Herbarium) Origin
M. latifolia Davis 639 (L) Indonesia, Papua C, D HG971215 HG971382 HG971533 HG971678
M. latifolia Curry 1314 (L) Vanuatu C, D HG971216 HG971383 HG971534 HG971088 HG971679
M. lauterbachii Whistler 1148 (B) Samoa F MG668989 MG595158 MG668945 –
M. lucida Meyer 808 Tahiti F HG971217 HG971384 HG971535 HG971089 HG971680
M. lucida Florence 11461 (US) Tahiti F MG595168 MG668946 –
M. lunu-ankenda Stone 16055 (US) Malaysia B, C HG971218 HG971385 HG971536
M. macrocarpa Kato 20120215150 (MAK) Malaysia B, C AB766285 AB766284 AB766287
M. madagascariensis Ramananjanakary 410 (MO) Madagascar A HG971219 HG971386 HG971537 HG971090 HG971681
M. madagascariensis Schatz 4057 (MO) Madagascar A HG971220 HG971387 HG971538 HG971091 HG971682
M. makahae Wagner 6904 (US) Hawaii, O‘ahu G HG002821 þ
HG002897
HG002441 HG002576 HG002691 HG003004
M. mantellii Pelser 3122 (GOET) New Zealand D MG668990 MG595159 MG668947 MG668960 MG668971
M. mantellii Gardner 670 (L) New Zealand D MG668991 MG595160 MG668948 MG668961 MG668972
M. margaretae Meyer 1003 (NY) Austral Islands F HG971221 HG971388 HG971539 HG971092 HG971683
M. margaretae Perlman 17954 (NY) Austral Islands F HG971222 HG971389 HG971540 HG971093 HG971684
M. maxii Brambach 1916 (GOET) Indonesia, Sulawesi C MG668992 MG595161 MG668949 MG668962 MG668973
M. micrococca Carroll 941 (CANB) Australia D HG971223 HG971390 HG971541 HG971685
M. molokaiensis Oppenheimer 60150 (US) USA, Hawaii, Maui G HG002822 þ
HG002898
HG002442 HG002577 HG002692 HG003005
M. molokaiensis Oppenheimer 80023 (US) USA, Hawaii, Maui G HG002823 þ
HG002899
HG002443 HG002578 HG002693 HG003006
M. molokaiensis Wagner 6911 (US) USA, Hawaii, O‘ahu G HG002762 HG002444 HG002579 HG002694 HG003007
M. mucronata Takeuchi 19705 (L) Papua New Guinea D HG971297 HG971391 HG971542
M. mucronata Appelhans 442 (LAE, US) Papua New Guinea D HG971543 HG971686
M. mucronata Appelhans 443 (US) Papua New Guinea D HG971224 HG971392 HG971544
M. mucronulata Wood 7041 (PTBG) USA, Hawaii, Moloka‘i G HG002824 þ
HG002900
HG002445 HG002580 HG002695 HG003008
M. munroi Wood 12749 (PTBG) USA, Hawaii, L
ana‘i G HG002763 HG002446 HG002581 HG002696 HG003009
M. nishimurae 404831 (MAK) Japan, Anijima Island E AB766373 AB766372 AB766375
M. nishimurae 404832 (MAK) Japan, Anijima Island E AB766377 AB766376 AB766379
M. nishimurae 404829 (MAK) Japan, Anijima Island E AB766365 AB766364 AB766367
M. nishimurae 404830 (MAK) Japan, Anijima Island E AB766369 AB766368 AB766371
M. novoguineensis Takeuchi 24615 (LAE) Papua New Guinea D HG971453 HG971611
M. nukuhivensis Meyer 889 Marquesas Islands F EU493232 EU493175 HG002582 EU493194 HG003010
M. oahuensis Wagner 6899 (US) USA, Hawaii, O‘ahu G HG002825 þ
HG002901
HG002447 HG002583 HG002697 HG003011
Continued
Pacific biogeography of Melicope (Rutaceae) 9
www.jse.ac.cn J. Syst. Evol. 9999 (9999): 1–24, 2018
Table 1 Continued
Taxon Voucher information Area
code
trnL-trnF ITS ETS psbA-trnH NIAi3
Collector & number (Herbarium) Origin
M. oahuensis Wagner 6902 (US) USA, Hawaii, O‘ahu G HG002826 þ
HG002902
HG002448 HG002584 HG002698 HG003012
M. oahuensis Wagner 6910 (US) USA, Hawaii, O‘ahu G HG002764 HG002449 HG002585 HG002699 HG003013
M. oblanceolata Appelhans 461 (LAE, US) Papua New Guinea D HG971279 HG971393 HG971545 HG971094 HG971687
M. oblanceolata Appelhans 462 (LAE, US) Papua New Guinea D HG971394 HG971546 HG971095 HG971688
M. obscura Larsen OBS1 (C) La R
eunion A HG971225 HG971395 HG971547 HG971096 HG971689
M. obtusifolia Olsen s.n. (C) La R
eunion A HG971226 HG971396 HG971548 HG971097 HG971690
M. orbicularis Oppenheimer 60087 (US) USA, Hawaii, Maui G HG002827 þ
HG002903
HG002450 HG002586 HG002700 HG003014
M. orbicularis Wood 14762 (PTBG) USA, Hawaii, Maui G HG002765 HG002451 HG002587 HG002701 HG003015
M. orbicularis Wood 2739 (PTBG) USA, Hawaii, Maui G HG002766 HG002452 HG002588 HG002702 HG003016
M. ovalis Wood 13724 (PTBG) USA, Hawaii, Maui G HG002828 þ
HG002904
HG002453 HG002589 HG002703 HG003017
M. ovalis Wood 7682 (PTBG) USA, Hawaii, Maui G EU493226 EU493169 HG002590 EU493188 HG003018
M. ovata Perlman 15244–Seed and DNA collec-
tion without voucher
USA, Hawaii, Kaua‘i G HG002767 HG002454 HG002591 HG002704 HG003019
M. ovata Wagner 6897 (US) USA, Hawaii, Kaua‘i G HG002768 HG002455 HG002592 HG002705 HG003020
M. ovata Wood 13850 (PTBG) USA, Hawaii, Kaua‘i G HG002829 þ
HG002905
HG002456 HG002593 HG002706 HG003021
M. pachyphylla Kato 20120216163 (MAK) Malaysia B AB766289 AB766288 AB766291
M. pachypoda James 326 (LAE, BISH, GOET) Papua New Guinea D HG971227 HG971397 HG971549 HG971098 HG971691
M. pachypoda Appelhans 417 (LAE, US) Papua New Guinea D HG971228 HG971398 HG971550 HG971099 HG971692
M. pachypoda Appelhans 447 (LAE, US) Papua New Guinea D HG971229 HG971399 HG971551 HG971100 HG971693
M. pallida Wood 7366-A (PTBG) USA, Hawaii, Kaua‘i G HG002830 þ
HG002906
HG002457 HG002594 HG002707 HG003022
M. pallida Perlman 19410 (PTBG) USA, Hawaii, Kaua‘i G HG002831 þ
HG002907
HG002458 HG002595 HG002708 HG003023
M. paniculata Perlman 18693 (PTBG) USA, Hawaii, Kaua‘i G HG002832 þ
HG002908
HG002459 HG002596 HG002709 HG003024
M. paniculata Wood 13686 (PTBG) USA, Hawaii, Kaua‘i G HG002833 þ
HG002909
HG002460 HG002597 HG002710 HG003025
M. paniculata Wood 7340 (PTBG) USA, Hawaii, Kaua‘i G EU493228 EU493171 HG002598 EU493190 HG003026
M. paniculata Wood 8234 (PTBG) USA, Hawaii, Kaua‘i G HG002834 þ
HG002910
HG002461 HG002599 HG002711
M. peduncularis Wagner 6905 (US) USA, Hawaii, O‘ahu G HG002769 HG002462 HG002600 HG002712 HG003027
M. peduncularis Wagner 6909 (US) USA, Hawaii, O‘ahu G HG002835 þ
HG002911
HG002463 HG002601 HG002713 HG003028
Continued
10 Appelhans et al.
J. Syst. Evol. 9999 (9999): 1–24, 2018 www.jse.ac.cn
Table 1 Continued
Taxon Voucher information Area
code
trnL-trnF ITS ETS psbA-trnH NIAi3
Collector & number (Herbarium) Origin
M. polyadenia Appelhans 438 (LAE, US) Papua New Guinea D HG971230 HG971400 HG971552 HG971101 HG971694
M. polyadenia James 661 (BISH, GOET) Papua New Guinea D HG971231 HG971401 HG971553 HG971102 HG971695
M. polybotrya Hutton 284 (CANB) Lord Howe Island D EU493240 EU493183 HG971554 EU493202 HG971696
M. ponapensis Tangalin 1182 (PTBG) Caroline Islands, Pohnpei E HG971232 HG971402 HG971555
M. ponapensis Tangalin 1208 (PTBG) Caroline Islands, Pohnpei E HG002770 HG002464 HG002602 HG002714 HG003029
M. pteleifolia de Wilde 6812 (L) Thailand B HG971233 HG971403 HG971556 HG971103 HG971697
M. pteleifolia de Wilde 6786 (L) Thailand B HG002836 þ
HG002912
HG002465 HG002603 HG002715 HG003030
M. pteleifolia Wen 11376 (US) China B HG971234 HG971404 HG971557 HG971104 HG971698
M. pteleifolia Zhou 1046 (KUN) China B HG971235 HG971405 HG971558 HG971105 HG971699
M. pteleifolia GSBS 31117 (GH) China, Yunnan B MG668993 MG595162 MG668950 MG668963 MG668974
M. pteleifolia Van den Bult 1186 (M) Thailand B MG668981 MG668951 MG668975
M. puberula Wagner 6895 (US) USA, Hawaii, Kaua‘i G EU493229 EU493172 HG002604 EU493191 HG003031
M. puberula Wood 14144 (PTBG) USA, Hawaii, Kaua‘i G HG002837 þ
HG002913
HG002466 HG002605 HG002716
M. puberula Wood 7438 (PTBG) USA, Hawaii, Kaua‘i G HG002838 þ
HG002914
HG002467 HG002606 HG002717
M. puberula Wood 7448 (PTBG) USA, Hawaii, Kaua‘i G HG002839 þ
HG002915
HG002468 HG002607 HG002718 HG003032
M. puberula Wood 8252 (PTBG) USA, Hawaii, Kaua‘i G HG002771 HG002469 HG002608 HG002719 HG003033
M. puberula Wood 8255 (PTBG) USA, Hawaii, Kaua‘i G HG002840 þ
HG002916
HG002470 HG002609 HG002720
M. quadrangularis Wood 0859 (PTBG) USA, Hawaii, Kaua‘i G EU493227 EU493170 HG002610 EU493189
M. quadrilocularis 404833 (MAK) Japan, Chichijima Island E AB766361 AB766360 AB766363
M. quadrilocularis Katoh B128 (MAK) Japan, Chichijima Island E AB766357 AB766356 AB766359
M. radiata Wagner 5966 (US) USA, Hawaii, Hawai‘i G HG002841 þ
HG002917
HG002472 HG002612 HG002722 HG003035
M. radiata Wood 12335 (PTBG) USA, Hawaii, Hawai‘i G HG002842 þ
HG002918
HG002473 HG002613 HG002723 HG003036
M. radiata Wood 12345 (PTBG) USA, Hawaii, Hawai‘i G HG002843 þ
HG002919
HG002474 HG002614 HG002724 HG003037
M. reflexa Wood 7419 (PTBG) USA, Hawaii, Maui G HG002772 HG002475 HG002615 HG002725 HG003038
M. reflexa Wood 7408 (PTBG) USA, Hawaii, Maui G HG002773 HG002476 HG002616 HG002726 HG003039
M. remyi Perlman 17674 (PTBG) USA, Hawaii, Hawai‘i G HG002858 þ
HG002937
HG002505 HG002645 HG002749 HG003060
M. retusa Whistler 6676 (US) Polynesia, Tonga F HG002774 HG002477 HG002617 HG002727 HG003040
M. revoluta Meyer 888 Marquesas islands F EU493231 EU493174 HG002618 EU493193
Continued
Pacific biogeography of Melicope (Rutaceae) 11
www.jse.ac.cn J. Syst. Evol. 9999 (9999): 1–24, 2018
Table 1 Continued
Taxon Voucher information Area
code
trnL-trnF ITS ETS psbA-trnH NIAi3
Collector & number (Herbarium) Origin
M. rhytidocarpa Gideon 20131 (L) Papua New Guinea D MG668994 MG595163 MG668952 MG668964 MG668976
M. richii Whistler 3664 (B) Samoa F MG668995 MG595164 MG668953 MG668965 MG668977
M. rostrata Wood 14210 (PTBG) USA, Hawaii, Kaua‘i G HG002859 þ
HG002938
HG002506 HG002646 HG002750 HG003061
M. rostrata Wood 8223 (PTBG) USA, Hawaii, Kaua‘i G EU493238 EU493181 HG002647 EU493200 HG003062
M. rotundifolia Wagner 6901 (US) USA, Hawaii, O‘ahu G HG002844 þ
HG002920
HG002478 HG002619 HG002728 HG003041
M. rotundifolia Wood 4133 (PTBG) USA, Hawaii, O‘ahu G HG002775 HG002479 HG002620 HG002729 HG003042
M. rubra Takeuchi 20069 (L) Papua New Guinea D HG971280 þ
HG971298
HG971406 HG971559 HG971106
M. rubra James 612 (LAE, BISH, GOET) Papua New Guinea D HG971236 HG971407 HG971560 HG971107 HG971700
M. rubra Appelhans 425 (LAE, US) Papua New Guinea D HG971237 HG971408 HG971561 HG971108 HG971701
M. rubra Appelhans 397 (US) cultivated SING (Nr.
0010298L)
D HG971238 HG971409 HG971562 HG971109 HG971702
M. rubra (aff.) Takeuchi 19249 (L) Papua New Guinea D MG668979 MG595155 MG668942 –
M. sambiranensis Antilahimena 4763 (MO) Madagascar A HG971281 þ
HG971299
HG971410 HG971563 HG971110 HG971703
M. schraderi Johns 9022 (L) Papua New Guinea D HG971239 HG971411 HG971564
M. schraderi Appelhans 421 (US) Papua New Guinea D HG971240 HG971412 HG971565 HG971111 HG971704
M. schraderi Appelhans 444 (LAE, US) Papua New Guinea D HG971241 HG971413 HG971566 HG971112 HG971705
M. schraderi Appelhans 445 (LAE, US) Papua New Guinea D HG971242 HG971414 HG971567 HG971113 HG971706
M. semecarpifolia Wagner 6588 (US) China, Taiwan B HG971243 HG971415 HG971568 HG971114 HG971707
M. semecarpifolia Sugawara 2012080812 (MAK) China, Taiwan B AB766281 AB766280 AB766283
M. sessilis Oppenheimer 60138 (US) USA, Hawaii, Maui G HG002845 þ
HG002921
HG002480 HG002621 HG002730
M. sessilis Oppenheimer 80004 (US) USA, Hawaii, Maui G HG002776 HG002481 HG002622 HG002731
M. sessilis Perlman 15706 (PTBG) USA, Hawaii, Maui G HG002777 HG002482 HG002623
M. sessilis Wagner 6913 (US) USA, Hawaii, O‘ahu G HG002778 HG002483 HG002624 HG002732 HG003043
M. sessilis Wood 14769 (PTBG) USA, Hawaii, Maui G HG002846 þ
HG002922
HG002484 HG002625 HG002733 HG003044
M. sessilis Wood 6207 (PTBG) USA, Hawaii, Maui G HG002779 HG002485 HG002626 HG002734 HG003045
M. simplex Gardner 3188 (L) New Zealand D HG002847 þ
HG002923
HG002486 HG002627 HG002735 HG003046
M. simplex Pelser 3121 (GOET) New Zealand D MG668996 MG595165 MG668954 MG668966 MG668978
M. sororia Beaman 9611 (US) Borneo B, C HG971244 HG971416 HG971569 HG971115 HG971708
M. sororia Appelhans 384 (US) Borneo B, C HG971245 HG971417 HG971570 HG971116 HG971709
M. spathulata Wagner 6893 (US) USA, Hawaii, Kaua‘i G EU493239 EU493182 HG002648 EU493201 HG003063
Continued
12 Appelhans et al.
J. Syst. Evol. 9999 (9999): 1–24, 2018 www.jse.ac.cn
Table 1 Continued
Taxon Voucher information Area
code
trnL-trnF ITS ETS psbA-trnH NIAi3
Collector & number (Herbarium) Origin
M. spathulata Wood 12723 (PTBG) USA, Hawaii, Kaua‘i G HG002785 HG002507 HG002649 HG002751 HG003064
M. spathulata Wood 14213 (PTBG) USA, Hawaii, Kaua‘i G HG002860 þ
HG002939
HG002508 HG002650 HG002752 HG003065
M. spathulata Wood 8264 (PTBG) USA, Hawaii, Kaua‘i G HG002861 þ
HG002940
HG002509 HG002651 HG002753 HG003066
M. spec. Wood 7719 (PTBG) USA, Hawaii, Kaua‘i G HG002848 þ
HG002924
HG002487 HG002628 HG002736 HG003047
M. spec. Wood 8266 (PTBG) USA, Hawaii, Kaua‘i G HG002849 þ
HG002925
HG002488 HG002629 HG002737 HG003048
M. spec. Pitopang 1049 (GOET) Indonesia, Sulawesi MG668980 MG595169 MG668955 –
M. spec. Munzinger 785 (MO) New Caledonia D HG971282 HG971420 HG971573 HG971119
M. spec. NT 11847 (L) Indonesia, Papua HG971248 HG971421 HG971574 HG971120 HG971712
M. spec. Rakotovao 2873 (MO) Madagascar HG971249 HG971422 HG971575 HG971121 HG971713
M. spec. Ravelonarivo 1703 (MO) Madagascar HG971250 HG971423 HG971576 HG971122 HG971714
M. spec. Ravelonarivo 1781 (MO) Madagascar HG971251 HG971424 HG971577 HG971123 HG971715
M. spec. Munzinger 1111 (P) New Caledonia HG971300 HG971425 HG971578 HG971124 HG971716
M. spec. Munzinger 927 (P) New Caledonia D HG971252 HG971426 HG971579 HG971125 HG971717
M. spec. Appelhans 429 (LAE, US) Papua New Guinea HG971253 HG971427 HG971580
M. spec. Appelhans 446 (LAE, US) Papua New Guinea HG971254 HG971428 HG971581 HG971126 HG971718
M. stellulata Appelhans 427 (LAE, US) Papua New Guinea D HG971255 HG971429 HG971582 HG971127 HG971719
M. subunifoliolata Beaman 8948 (L) Borneo C HG971256 HG971430 HG971583 HG971128 HG971720
M. subunifoliolata Appelhans 383 (US) Borneo C HG971257 HG971431 HG971584 HG971129 HG971721
M. ternata Appelhans 487 (GOET) cultivated Botanical Garden
Goettingen
D HG971258 HG971432 HG971585 HG971130 HG971722
M. trachycarpa Appelhans 430 (LAE, US) Papua New Guinea D HG971259 HG971433 HG971586 HG971723
M. trachycarpa Appelhans 431 (LAE, US) Papua New Guinea D HG971260 HG971434 HG971587 HG971131 HG971724
M. trichantha Fosberg 47679 (NY) Caroline Islands E HG971261 HG971435 HG971588
M. triphylla Appelhans 394 (GOET) cultivated Hortus Botanicus
Leiden
C, D HG002780 HG002489 HG002630 HG002738 HG003049
M. triphylla Utteridge 252 (L) Indonesia, Papua C, D HG971262 HG971436 HG971589
M. vatiana Whistler 4170 (US) Samoa F HG002850 þ
HG002926
HG002490 HG002631 HG002739
M. vieillardii McPherson 18066 (MO) New Caledonia D HG002781 HG002491 HG002632 HG002740 HG003050
M. viticina Chantarasuwan 2011-01 (US) Thailand B HG971263 HG971437 HG971590 HG971132 HG971725
M. viticina Esser 11-47 (M) Thailand B HG971264 HG971438 HG971591 HG971133 HG971726
M. vitiflora Forster 29363 (L) Australia D HG002851 þ
HG002927
HG002492 HG002633 HG002741 HG003051
Continued
Pacific biogeography of Melicope (Rutaceae) 13
www.jse.ac.cn J. Syst. Evol. 9999 (9999): 1–24, 2018
Table 1 Continued
Taxon Voucher information Area
code
trnL-trnF ITS ETS psbA-trnH NIAi3
Collector & number (Herbarium) Origin
M. vitiflora (cf) Appelhans 433 (LAE, US) Papua New Guinea D HG971265 HG971439 HG971592 HG971134
M. volcanica Oppenheimer 100029 (US) USA, Hawaii, Maui G HG002782 HG002493 HG002634 HG002742 HG003052
M. volcanica Wood 13735 (PTBG) USA, Hawaii, Maui G HG002852 þ
HG002928
HG002494 HG002635 HG002743 HG003053
M. volcanica Wood 4650 (PTBG) USA, Hawaii, Hawai‘i G HG002853 þ
HG002929
HG002495 HG002636
M. volcanica Wood 6797 (PTBG) USA, Hawaii, Maui G HG002854 þ
HG002930
HG002496 HG002637
M. waialealae Wood 8148 (PTBG) USA, Hawaii, Kaua‘i G HG002855 þ
HG002931
HG002497 HG002638 HG002744 HG003054
M. waialealae Wood 8185 (PTBG) USA, Hawaii, Kaua‘i G HG002783 HG002498 HG002639 HG002745 HG003055
M. waialealae Wood 8233 (PTBG) USA, Hawaii, Kaua‘i G HG002856 þ
HG002932
HG002499 HG002640 HG003056
M. wawraeana Wood 7463 (PTBG) USA, Hawaii, Kaua‘i G HG002933 HG002500 HG002641 HG002746 HG003057
M. wawraeana Wood 8147 (PTBG) USA, Hawaii, Kaua‘i G HG002857 þ
HG002934
HG002501 HG002642 HG002747 HG003058
M. wawraeana Wood 7464 (PTBG) USA, Hawaii, Kaua‘i G HG002784 HG002502 HG002643 HG002748 HG003059
M. xanthoxyloides Takeuchi 15373 (L) Papua New Guinea D HG971301 HG971440 HG971593 HG971135
Ma. spec. John 145743 (L) Malaysia, Sabah B, C HG971289 HG971329 HG971483
Me. glandulosa Forster 25045 (L) Australia, Queensland D HG971172 HG971330 HG971484 HG971045
My. macrocarpa Van Balgooy 6955 (L) New Caledonia D MG668983 MG595166 – MG668956 –
My. myrtoidea McPherson 18026 (MO) New Caledonia D HG971283 HG971441 HG971136
My. spec. Lowry II 6464 (L) New Caledonia D MG668982 MG595167 – MG668957 –
Pe. parviflorum Pullen 7313 (US) Papua New Guinea D HG971267 HG971443 HG971595 HG971138
Pic. glandulosa McKee 3189 (US) New Caledonia D HG971268 HG971444 HG971597 HG971140 HG971727
Pic. glandulosa McPherson 18598 (MO) New Caledonia D HG971269 HG971445 HG971598 HG971141 HG971728
Pic. ignambiensis McPherson 19132 (MO) New Caledonia D HG971284 þ
HG971302
HG971446 HG971599 HG971142 HG971729
Pit. haplophyllus Ford 4821 (L) Australia, Queensland D HG971270 HG971447 HG971600 HG971143 HG971730
S. follicularis Munzinger 668 (MO) New Caledonia D, F HG971303 HG971448 HG971601 HG971144 HG971731
T. tetrandrum Beaman 8917 (L) Borneo C, D HG971271 HG971449 HG971602 HG971145 HG971732
T. tetrandrum Utteridge 544 (L) Papua New Guinea C, D MG668984 MG595152 MG668939 –
T. tetrandrum Utteridge 436 (L) Indonesia, Papua C, D LN849198 LN849159 LN849250 LN849176 LN849219
T. tetrandrum Brambach 1472 (GOET) Indonesia, Sulawesi C, D MG668985 MG595153 MG668940 – MG668967
Herbarium acronyms are according to Index Herbariorum (http://sweetgum.nybg.org/science/ih/). Specimens used for the AAR and the diversication analyses are marked in bold.
Abbreviations of genus names are: A.¼Acronychia,Bo.¼Boronella,Br. ¼Brombya,C. ¼Comptonella,D. ¼Dutaillyea,E.¼Euodia,Ma.¼Maclurodendron,Me.¼Medicosma,
M.¼Melicope,My.¼Myrtopsis,Pe. ¼Perryodendron,Pic.¼Picrella, Pit.¼Pitaviaster,S.¼Sarcomelicope,T.¼Tetractomia. For the denition of the area code see Fig. 1. Sequences
generated for this study are marked with .
14 Appelhans et al.
J. Syst. Evol. 9999 (9999): 1–24, 2018 www.jse.ac.cn
1981) represent Tetradium Lour. species, a genus only distantly
related to Melicope (Poon et al., 2007).
Since no reliable fossils were available, a secondary
calibration was used to constrain the root age. Appelhans
et al. (2012) used a dataset including all major lineages of
Rutaceae as well as all families of Sapindales for a molecular
dating analysis, employing four fossil calibration points. We
used the estimated split between Melicope and the Australian
Correa Andrews - Philotheca Rudge clade from Appelhans et al.
(2012) to constrain the root age in the present study.
Myrtopsis, the outgroup taxon in our study belongs to this
clade (Bayly et al., 2013). The prior for the root age was
assigned a normal distribution and was truncated to an upper
limit of 48.99 Ma (millions of years ago) and a lower limit of
35.61 Ma, reecting the 95% credibility interval for this split as
inferred by Appelhans et al. (2012).
The models of sequence evolution were set as in Table 2.
Two independent BEAST runs consisted of 50 million
generations each with tree sampling every 1000
th
generation.
A UPGMA starting tree was used, a lognormal relaxed clock
was applied and the tree prior was set to the birth-death
process. The resulting tree les contained 50 000 trees, and
we used LogCombiner v.1.8.4 (Drummond et al., 2012) to
resample states at lower frequency and thereby shrinking the
resulting tree les to 10 000 trees. Of these, ten percent were
discarded as burn-in using LogCombiner, and a maximum
clade credibility (MCC) tree was calculated in TreeAnnotator
v.1.8.4 (Drummond et al., 2012) after checking if effective
sample sizes (ESS) were above 200 for all parameters in Tracer
1.6.0 (Rambaut et al., 2014).
2.4 Ancestral area reconstruction
The BIOGEOBEARS package (Matzke, 2013) implemented in
R 3.1 was used for AAR.
Seven areas of endemism were delimited based on clusters
of distributions of member species of the clade. These areas
are similar to those based on wider assessments of oras of
the regions by Takhtajan (1986).
These areas are: (A) Madagascar and the Mascarene
Islands; (B) Mainland S & E Asia, including Hainan, Taiwan
and the Ryukyu Islands, excluding the Malay peninsula; (C)
Malesia; (D) Australasia (New Guinea to Vanuatu, Australia,
New Caledonia, New Zealand, Lord Howe Island, Kermadec
Islands); (E) Micronesia, Ogasawara and Bonin Islands; (F) Fiji
to Marquesas, Society, and Austral Islands; and (G) Hawaiian
Islands (Fig. 1).
For the AAR, each specimen was assigned to the
distribution area of the species, except for the genera
Maclurodendron,Medicosma,Sarcomelicope and Tetractomia
and the Melicope sororia T.G.Hartley clade. These taxa each
contain between ve to 22 species, but only one species each
was included in our analyses. We assigned the distribution
area of the whole taxon to the sampled specimen in order not
to neglect any geographical information. All other genera
were represented with species throughout their geographic
range. The outgroup taxa Boronia (section Boronella) and
Myrtopsis are representatives of large and mainly Australian
clades (Kubitzki et al., 2011; Bayly et al., 2013).
BIOGEOBEARS implements the two most frequently used
biogeographic models: the Dispersal-Vicariance (DIVA; Ron-
quist, 1997) model and the Dispersal-Extinction-Cladogenesis
(DEC) model (Ree & Smith, 2008). In addition, the BAYAREA
model is available in BioGeoBEARS, which resembles the
Bayesian Binary Model in RASP (Yu et al., 2015). These three
models can be modied by adding a factor “J” for founder-
event speciation or jump dispersal (Matzke, 2013, 2014) and
we compared the six models “DIVALIKE”, “DIVALIKEþJ”,
“DEC”, “DECþJ”, “BAYAREA” and “BAYAREAþJ”.
2.5 Diversification analyses
Diversication analyses were carried out using BAMM
(Bayesian Analysis of Macroevolutionary Mixtures; Rabosky
et al., 2014). To account for incomplete taxon sampling with
non-random distribution of missing taxa throughout the
phylogeny, all missing taxa were assigned to one of the major
clades based on morphological evidence (Hartley, 1974, 1983,
1984, 2001, 2013; Hartley & Mabberley, 2003). For this, the
dated phylogenetic tree based on the dataset that contains
only one sample per species was subdivided into 17 major
clades (Table 3). The numbers of species per clade are largely
different because several clades allowed assigning missing
taxa with high condence (e.g., “CD” clade), whereas the
uncertainty to place missing taxa in other clades was higher,
resulting in a broader denition of a group (e.g., “Le” clade).
For each clade, the percentage of sampled species was
calculated and used as input for BAMM (Table 3). As a control
to evaluate the effects of clade sizes, we did a BAMM analysis
in which the dataset was split up in only nine clades of similar
Table 2 Models of sequence evolution for all single marker alignments (full dataset and reduced dataset for Ancestral Area
Reconstruction in BioGeoBEARS and Diversication Analyses in BAMM) estimated using the Akaike Information Criterion (AIC)
algorithm in jModeltest 2.1.7 (Darriba et al., 2012)
trnL-trnF ITS ETS psbA-trnH NIAi3
Full dataset
Best AIC model TVM þIþG GTR þIþG TIM2 þG TVM þG TPM3uf þG
Best AIC model available for MrBayes GTR þIþG GTR þIþG GTR þG GTR þG GTR þG
Best AIC model available for BEAST GTR þIþG GTR þIþG GTR þG GTR þG GTR þG
BioGeoBEARS & BAMM dataset
Best AIC model TVM þG TIM2ef þIþG TIM2 þG TVM þG TIM3 þIþG
Best AIC model available for MrBayes GTR þG GTR þIþG GTR þG GTR þG GTR þIþG
Best AIC model available for BEAST GTR þG GTR þIþG GTR þG GTR þG GTR þIþG
The table shows the models with the highest likelihood scores and the highest available models available in MrBayes 3.2.5 and
BEAST v.1.8.4.
Pacific biogeography of Melicope (Rutaceae) 15
www.jse.ac.cn J. Syst. Evol. 9999 (9999): 1–24, 2018
size (clades CD, M2, NC, Sa and VP merged into one clade;
clades Ha, M1, Pe, Pl and So merged into one clade).
All BAMM analyses consisted of four Markov chain Monte
Carlo (MCMC) chains, which were run for 10 million
generations, with all other settings left at their defaults.
The visualization of the results was done using the R-package
‘BAMMtools’ (Rabosky et al., 2014).
3 Results
3.1 Phylogeny & molecular dating
The phylogenetic reconstructions are congruent with
Appelhans et al. (2014a, 2014b) and Holzmeyer et al. (2015)
and are not described or discussed in detail here. The
Acronychia-Melicope clade shows the same four main clades
as described by Appelhans et al. (2014a), and also the sister
relationships of Acronychia-Melicope with Medicosma, and of
Acronychia-Melicope-Medicosma with Tetractomia are sup-
ported (Figs. 2, S1).
The results of the BEAST analyses were congruent with the
MrBayes analysis. BEAST analyses based on the full dataset
and the smaller dataset, which included one specimen per
species were nearly identical except for the root age. The root
age of the full dataset was estimated to 35.6 Ma, while that of
the smaller dataset was 49.1 Ma and the credible intervals did
not overlap. However, all age estimates concerning the
ingroup showed differences of less than 1 Myr in the two
Fig. 1. Denition of areas and results of the Ancestral Area Reconstruction using BIOGEOBEARS. The dispersal events into the
Pacic are highlighted on the right. See 2.4 for the denitions of areas A to G. Source of the map: www.d-maps.com.
16 Appelhans et al.
J. Syst. Evol. 9999 (9999): 1–24, 2018 www.jse.ac.cn
datasets and only the age estimates of the full dataset are
described here. The oldest fossils that might belong to the
Acronychia-Euodia-Melicope group were not included in our
analyses because of their unclear afnities, but their ages are
congruent with our molecular dating results that suggest an
origin of the main lineages in the Late Oligocene to Mid
Miocene. This is congruent with other molecular dating
analyses in the order Sapindales (Manafzadeh et al., 2014;
Koenen et al., 2015; Muellner-Riehl et al., 2016).
The BEAST analyses (Fig. 2) supported the tree topology
of the Bayesian phylogenetic reconstruction (Fig. S1). The
Euodia clade dated back to Mid or Early Miocene with a
crown age of 17.3 Ma (credibility interval: 12.1–24.6 Ma). The
crown age marked the split between Perryodendron from
the remainder of the Euodia clade. Euodia (including
Pitaviaster,Brombya and Melicope vitiora) was also
estimated to be of Miocene origin (mean: 14.1 Ma; credibility
interval: 9.6–19.5 Ma).
The BEAST analysis supported Melicope and Acronychia as
close relatives and sister to Medicosma, and this clade
was then sister to Tetractomia. The Acronychia-Medicosma-
Melicope-Tetractomia clade started to diversify in the Late
Oligocene or Early Miocene (20.7 Ma; 15.0–26.9 Ma) and
the Acronychia-Medicosma-Melicope clade diversied later
(15.9 Ma; 11.3–21.3 Ma). Acronychia was nested within Melicope
in the BEAST MCC tree, but statistical support was lacking
(0.86 pp) and the clade dated from the Early to Late Miocene
(14.8 Ma; 10.6–19.8 Ma).
There were four main clades in the Acronychia-Melicope
group (¼clades 1 to 4 in Figs. 1, 2). Clade 1: Melicope section
Pelea (A.Gray) Hook.f. p.p., the former genus Platydesma, as
well as two clades of Melicope section Melicope p.p., was
estimated to have originated in the Late or Mid Miocene
(12.3 Ma; 8.5–16.9 Ma). Clade 2: section Lepta (Lour.) T.G.
Hartley, was slightly younger (9.6 Ma; 6.2–14.1 Ma). Clade 3:
Acronychia and Maclurodendron, dated to the Late Miocene
or Early Pliocene (4.9 Ma; 3.1–8.1 Ma). Within the
Acronychia-Maclurodendron clade, all early-branching clades
were Australian taxa, while all New Guinean and Malesian
species belonged to one clade that was estimated to the
Pliocene to Early Pleistocene (2.5 Ma; 1.5–4.1 Ma). Clade 4:
Melicope sections Melicope p.p. and Vitiorae T.G.Hartley
p.p., Sarcomelicope and several New Caledonian genera,
had a similar age as the species-rich clades 1 and 2 (9.9 Ma;
6.1–15.1 Ma).
The ages of several geographic clades were of particular
interest. The Malagasy and Mascarene species were mono-
phyletic within clade 2 with an origin in the Pliocene or Early
Pleistocene (2.8 Ma; 1.7–4.4 Ma). Within this clade, the
specimens from La R
eunion and Mauritius formed a clade,
which was dated to the Pleistocene (0.8 Ma; 0.3–1.7 Ma).
Clade 4 contained a high proportion of taxa from New
Caledonia. All New Caledonian subclades are dated to the Mid
Miocene to Early Pliocene.
The Hawaiian clade that also contained all species from the
Marquesas Islands had a stem age from the Mid or Late
Table 3 Denitions of clades specied in the BAMM analysis and the numbers and percentages of included and missing taxa. For
the exact placement of the clades in the phylogenetic trees, see Fig. 4
Clade name Description of included taxa Total number of taxa
(included þmissing)
Number of
missing taxa
Percentage of
missing taxa
Percentage of
included taxa
Ac Acronychia & Maclurodendron 55 31 0.56 0.44
CD Comptonella, Dutaillea, Dutailliopsis 11 6 0.55 0.45
Eu Euodia incl. M. vitiflora, Pitaviaster,
Brombya
11 4 0.36 0.64
Ha Hawaiian & Marquesas Melicope sec-
tion Pelea
55 15 0.27 0.73
Le Melicope section Lepta 102 64 0.63 0.37
M1 Melicope section Melicope part 1 28 20 0.71 0.29
M2 Melicope section Melicope 2 (incl.
type species)
6 1 0.17 0.83
Me Medicosma 22 21 0.95 0.05
NC New Caledonian Melicope section
Pelea
5 2 0.40 0.60
Pd Perryodendron 1 0 0.00 1.00
Pe Non-Hawaiian/Marquesas, non-New--
Caledonian Melicope section Pelea
25 14 0.56 0.44
Pl Platydesma 4 0 0.00 1.00
Sa Sarcomelicope 9 8 0.89 0.11
So Melicope sororia and relatives 5 4 0.80 0.20
Te Tetractomia 6 5 0.83 0.17
VP Melicope section Vitiflorae pro parte
plus Picrella
10 5 0.50 0.50
Total ingroup Acronychia-Euodia-Melicope clade 355 200 0.56 0.44
Outgroups Boronella & Myrtopsis
Pacific biogeography of Melicope (Rutaceae) 17
www.jse.ac.cn J. Syst. Evol. 9999 (9999): 1–24, 2018
Miocene (10.0 Ma; 6.8–14.3 Ma), while the diversication
began in the Late Miocene or Early Pliocene (7.5 Ma; 4.7–11.7
Ma). Compared to the Hawaiian clade, all other Pacic clades
are relatively young with estimated origins in the Pleistocene.
3.2 Ancestral area reconstruction
The comparison of the six available methods revealed that the
DECþJ model suited our dataset the best. Adding jump
dispersal (J) increased the likelihood of the AAR in all cases
(DEC, DIVALIKE, BAYAREA) (Table 4).
The AAR clearly identied Australasia (area D) as the
geographic origin of both the Acronychia-Melicope clade and
the Euodia clade (Fig. 1). Within the Euodia clade, only the
widespread species E.hortensis J.R.Forst. & G.Forst. colonized
areas outside Australasia, and it is also found in the South
Pacic area F.
The Acronychia-Melicope clade showed a more complex
biogeographic pattern. In clade 1 (Fig. 1), the Hawaiian lineage
was sister to the remainder of section Pelea, and our results
suggested an origin of the Hawaiian lineage from an
Australasian ancestor (colonization number 1 in Fig. 3). A
second lineage from clade 1, containing species from Pohnpei,
Samoa, Wallis & Futuna, Tonga and Niue (number 2 in Fig. 3)
dispersed eastward. Clade 2 (Fig. 1) did not disperse far into
the Pacic Ocean and only three species colonized Fiji, Tonga
and Samoa (numbers 7 to 9 in Fig. 3). Members of clade 2 also
colonized the North Pacic. The widespread Melicope
denhamii (Seem.) T.G.Hartley reaches its northern limit in
the Philippines and is also found on Palau and Pohnpei
(numbers 3 and 6 in Fig. 3). A second lineage colonized Palau
and the Ogasawara and Volcano Islands, respectively
(numbers 4 and 5 in Fig. 3). A larger lineage colonized Malesia
(area C) and mainland southern Asia (area B) as far west as
southern India and Sri Lanka. This lineage gave rise to the
Malagasy and Mascarene species (area A). Clade 3 (Fig. 1) was
of Australasian origin and most of the species are endemic to
Fig. 2. Molecular dating of the Acronychia-Euodia-Melicope clade using BEAST. The maximum clade credibility consensus tree is
shown with the credibility intervals of the age estimations displayed as bars. Important nodes are highlighted and their mean age
estimates and credibility interval (in brackets) are shown. Colored bars indicate the four sections of Melicope, and the positions of
other genera are marked with arrows. Abbreviations of genus names are: Com. ¼Comptonella, Dut. ¼Dutaillyea, Maclurod. ¼
Maclurodendron, Sarcomel. ¼Sarcomelicope.
18 Appelhans et al.
J. Syst. Evol. 9999 (9999): 1–24, 2018 www.jse.ac.cn
New Guinea and Australia. Only two lineages extend from
Australasia. These are: A.trifoliolata Zoll. & Moritzi, which
reaches its westernmost distribution in Java, and the A.
pedunculata Miq. and Maclurodendron clade, which occurs
from New Guinea to India and Sri Lanka. Clade 4 contains
mostly species from New Caledonia and this clade dispersed
into the South Pacic at least twice (numbers 10 and 11 in
Fig. 3). Both dispersal events led to the colonization of the
Society and Austral Islands.
3.3 Diversification analyses
The diversication analyses were visualized as a heatmap
plotted on the time-calibrated phylogenetic tree and as a
lineage-through-time plot (Fig. 4). The heatmap (Fig. 4A)
showed clades in colors according to their relative diversica-
tion rates and blue colors indicated low rates, while red colors
identied high rates. The lowest relative diversication rates
can be observed for the Euodia clade (clades Eu and Pd in
Fig. 4). Also Tetradium (Te) and Medicosma (Me), the
successive sister groups to the Acronychia-Melicope clade,
exhibit low relative diversication rates. Medium relative
diversication rates characterize the mainly New Caledonian
clade (CD, M2, NC, Sa, VP). Medium to higher relative
diversication rates are found in the three sister clades (M1,
So, Pe) to the Hawaiian taxa and in section Lepta (Le). The
highest relative diversication rates were found in two young
clades: the Acronychia-Maclurodendron clade (Ac) and espe-
cially the Hawaiian clade (Ha).
On average, the lineage-through-time plot (Fig. 4B) showed
a relatively constant diversication. This was interrupted by
two phases with increased relative diversication rates
(marked with orange bars in Fig. 4). The rst phase lasted
from about 18 to 14 Ma and marked the timeframe in which
the major lineages of the Acronychia-Euodia-Melicope clade
originated. The second phase started at about 3.5 to 4 Ma and
lasted until now. The major part of the diversication within
the Acronychia-Maclurodendron clade (Ac) and the Hawaiian
clade (Ha) fell within this phase.
The second BAMM analysis, in which the dataset was
subdivided into nine instead of 16 clades, delivered identical
results.
4 Discussion
4.1 Origin and the ages of the Acronychia-Euodia-Melicope
group
Our ancestral area reconstruction clearly suggests an Austral-
asian origin of the Acronychia-Euodia-Melicope group. Broader
phylogenetic studies of Rutaceae showed that Acronychia
and Melicope are part of a larger clade of mainly Australasian
genera (Groppo et al., 2008; Appelhans et al., 2012; Bayly
et al., 2013) and the three successive sister clades to the
Table 4 Comparison of the six models for Ancestral Area
Reconstruction
Model LnL
DEC –214.7720
DEC þJ –204.5273
DIVALIKE –223.0560
DIVALIKE þJ –211.6971
BAYAREA –248.3574
BAYAREA þJ –208.7406
Fig. 3. Dispersal patterns of Melicope in the Pacic inferred from the Ancestral Area Reconstruction. Arrows in dark gray refer to
lineages from clade 1, black arrows indicate lineages from clade 2, and light gray arrows are for lineages from clade 4 (see Figs. 1,
2, S1). An alternative pathway for the colonizations of Palau, Pohnpei, Ogasawara and Volcano Islands (black arrows) would be
from the Philippines instead of New Guinea. The numbers (1-11) refer to those mentioned in the results section (3.2). The question
mark and the dashed line indicate that it is unclear whether the colonization to New Caledonia is from an Australian or New
Guinean ancestor. Source of the map: www.d-maps.com.
Pacific biogeography of Melicope (Rutaceae) 19
www.jse.ac.cn J. Syst. Evol. 9999 (9999): 1–24, 2018
Acronychia-Euodia-Melicope group are Australasian and mostly
endemic to Australia (Bayly et al., 2013). The reconstruction of
Australasia as the geographic origin of the Acronychia-Euodia-
Melicope group is therefore not surprising.
While species of the Euodia clade and clades 3 and 4 (Fig. 1)
are mainly restricted to Australasia, several lineages of clades 1
and 2 moved out of Australasia. In clade 1, three lineages
moved out of Australasia. One lineage migrated into Malesia
in the Late or Mid Miocene (10.9 Ma; 7.3–15.6 Ma; Fig. 2). This
lineage consists of M. sororia and putatively ve morphologi-
cally similar species that have not been sampled. This group
colonized an area from Borneo to Hainan (China) and
southern India (Hartley, 2001). The other two migrations
relate to Pacic lineages, which will be discussed in the next
section. The westward migration from Australasia in clade 2
(Fig. 1) is more complex, however, the number and timing of
these migrations cannot be determined with condence
because of low statistical support of several subclades and the
present low sampling of species from Sumatra and the
Philippines. Clade 2 contains at least two well-supported
subclades mainly from Malesia and mainland SE Asia. Their
divergences from the Australasian lineages are dated to the
Late Miocene to Pliocene (6.0 Ma; 4.1–8.4 Ma; and 4.9 Ma;
3.5–6.7 Ma; Fig. 2). The slightly younger subclade also contains
the Malagasy and Mascarene species of Melicope. The closest
relatives of these species are M. glomerata (Craib) T.G.Hartley
and M. vicitina (Wall. ex Kurz) T.G.Hartley from mainland SE
Asia and the split of the Malagasy and Mascarene lineage
from these two species was dated to the Pliocene (3.4 Ma;
2.0–5.0 Ma; Fig. 2). This disjunction is one of the many
examples of biogeographic connections of tropical Asia and
Madagascar (Schatz, 1996).
Fig. 4. Results of the diversication analyses. The lineage-through-time plot is displayed with time in millions of years on the x-axis
and relative diversication rates on the y-axis. Two epochs with major shifts in diversication rates are highlighted in orange (B).
The branches in the phylogenetic tree are colored by their relative diversication rates, and red/orange colors represent high
diversication rates whereas blue colors indicate low diversication rates. See Table 3 for denitions of the clade names (A).
20 Appelhans et al.
J. Syst. Evol. 9999 (9999): 1–24, 2018 www.jse.ac.cn
4.2 Dispersal routes in the Pacific
Our analyses suggest numerous independent dispersal
events across the Pacic archipelagos in the Acronychia-
Euodia-Melicope group (Figs. 1, 3).
The Solomon Islands, Vanuatu and New Caledonia
played a crucial role in the diversication of the
Acronychia-Euodia-Melicope group in the South Pacic.
Within Euodia only one species (E. hortensis) colonized
areas east of Vanuatu. Pacic Islanders utilize this species
for its strong fragrance and for medicinal proposes. Its
occurrence east of Fiji might not be natural, as it is found
there only in cultivation and disturbed areas (Smith, 1985;
Hartley, 2001). The Acronychia-Melicope clade contains
many New Caledonian endemics (Fig. 1, clade 4) and New
Caledonia was the origin of several dispersal events deeper
into the Pacic Ocean. One dispersal event to New Zealand
resulted in three species, of which one is also found on the
Kermadec Islands. This New Zealand lineage also colonized
Tahiti (2 spp.) and the remote Austral Islands (1 sp.). A
second lineage of New Caledonian ancestry colonized Fiji,
and the Cook, Society and Austral Islands; and Tahiti and
the Austral Islands have thus been colonized twice
independently. Within the New Caledonian lineage (clade
4), two independent colonization events for Lord Howe
Island are inferred. The rst colonization corresponds to
the widespread species Sarcomelicope simplicifolia (Endl.)
T.G.Hartley, which also occurs from eastern Australia to Fiji
(Hartley, 1982). The second colonization refers to the Lord
Howe endemic M. polybotrya (C.Moore & F.Muell.) T.G.
Hartley (Hartley, 2001). One additional colonization event
to Lord Howe Island occurred in clade 2 (M. contermina C.
Moore & Muell.) and is probably derived from an Australian
ancestor. Australia is the most important source area for
the Lord Howe Island ora, so is New Caledonia’s role as a
major source area (Papadopulos et al., 2011). Melicope
(including Sarcomelicope) is the only known plant genus
with three independent colonizations into Lord Howe
Island.
With ten species, Samoa has the second highest number
of Acronychia-Euodia-Melicope species in the Pacic. In
addition to the widespread species E. hortensis and
M.latifolia (DC.) T.G.Hartley, the remaining species from
Samoa belong to section Pelea (clade 1, Fig. 1) and ve out of
eight species have been sampled here. These ve species
form a clade, and are therefore probably the result of a
single colonization event. Melicope sulcata T.G.Hartley, one
of the Samoan species that could not be sampled here, is
morphologically different from other Samoan species
(Hartley, 2001) and might be the result of an independent
colonization event. The Samoan clade is sister to M.
ponapensis Lauterb. from Pohnpei (Caroline Islands), which
is supported by morphology (Hartley, 2001). The closest
relatives of this clade are from New Guinea (Fig. S1), which is
likely the ancestral area of this group. The Caroline Islands
(Pohnpei and Kosrae) were colonized a second time by the
widespread M. denhamii (clade 2, Fig. 1). This species also
colonized Palau and in turn, Palau was colonized by a second
lineage. This lineage consists of two endemic species, which
are related to the widespread M. latifolia in clade 2
(Appelhans et al., 2014a; Fig. 1). The Japanese Ogasawara
and Volcano Islands represent the northernmost
colonization of Melicope in the Pacic. The three endemic
species are most likely the result of a single colonization
event either from New Guinea or the Philippines (Figs. 1, 3).
By far the most species-rich lineage within Melicope is the
Hawaiian radiation with 55 endemic species (Wood et al.,
2017). The seven species from the Marquesas Islands are part
of the Hawaiian lineage (Fig. 1), but belong to two different
subclades, supporting two colonization events to the
Marquesas Islands.
Most colonization events in the Pacic region east of the
andesite line are dated to the Pleistocene (Fig. 2) and all
archipelagos, on which Melicope species occur, were already
present in the Pleistocene (Clouard & Bonneville, 2005; Neall &
Trewick, 2008). The Hawaiian Islands represent the only
archipelago, for which our molecular dating results conict
with the age of islands. The stem age of Hawaiian Melicope is
dated to the Mid or Late Miocene, while the oldest of the
current main islands are about 5 Myr old (Price & Clague, 2002;
Neall & Trewick, 2008). The Hawaiian Islands are part of the
Hawaiian-Emperor seamount chain and other islands of the
chain were present in the Mid to Late Miocene. The initial
colonization of the Hawaiian Islands might have occurred on
the Gardner Pinnacles, French Frigate Shoals, Necker or Nihoa,
which are now low islands with depauperate vegetation
(Amerson, 1975; Price & Clague, 2002). Since only small and
distantly spaced islands were present at the Hawaiian-
Emperor seamount chain when Kaua‘i formed, Price & Clague
(2002) hypothesized a ‘bottleneck’ for colonization between 8
and 5 Ma. This bottleneck is supported by molecular dating
analyses: most Hawaiian lineages have crown ages of 5 Ma or
less (Keeley & Funk, 2011). Nevertheless, some Hawaiian
lineages, most notably the Drosophila Fall
en (Russo et al.,
1995) and Lobeliad (Givnish et al., 2009) lineages, have
estimated ages older than the current main islands, like in
Melicope. Thus at least some lineages were able to get
through the bottleneck. The age estimates for Melicope
further suggest that the split between the two major
Hawaiian clades (Melicope section Pelea and the former
genus Platydesma) occurred on one of the leeward islands.
The largely New Caledonian clade (clade 4; Figs. 1, 2) has an
estimated crown age in the Mid to Late Miocene. This
estimation is in agreement with the hypothesis that New
Caledonia was re-colonized via oceanic dispersals after being
submerged from the Late Cretaceous to about 37 Ma (Pillon,
2012).
4.3 Differences in diversification rates
The crown ages of the Euodia clade and the Acronychia-
Melicope clade are estimated to be of a nearly identical age
(Mid to Early Miocene; 17.3 Ma; 12.1–24.6 Ma vs. 14.8 Ma;
10.6–19.3 Ma). The Euodia clade contains about 12 species,
while the Acronychia-Melicope clade consists of more than 315
species (Kubitzki et al., 2011). With the close relationship
among Zieria,Neobyrnesia and the Euodia clade, and that of
Boronia section Cyanothamnus with the Acronychia-Melicope
clade (Duretto M, unpublished data) considered, this ratio
would be about 72 versus more than 338 species (Kubitzki
et al., 2011). This large difference in species richness is
reected in the distribution of the two groups. While the
Acronychia-Melicope clade is widely distributed from Mada-
gascar to the Hawaiian Islands (Fig. 1), the Euodia clade is only
Pacific biogeography of Melicope (Rutaceae) 21
www.jse.ac.cn J. Syst. Evol. 9999 (9999): 1–24, 2018
from the Moluccas in the west to Samoa and Niue in the east
(Hartley, 1997, 2001) and its occurrence east of Fiji might not
be natural (Smith, 1985). Most species of the Euodia clade
grow in ever-wet tropical rainforest up to 1200 m, and only
two reach higher altitudes of up to 2250 m (Hartley, 1997,
2001, 2013). Most species of the Acronychia-Melicope clade are
from tropical regions. However, some lineages colonized
subtropical areas in Australia and New Zealand (Hartley, 2001).
While most species occur in rainforests, several species have
adapted to other vegetation types including monsoon forests,
savannahs, Eucalyptus L’H
er. woodlands, subalpine shrub-
lands, alpine grasslands and bogs (Wagner et al., 1990;
Hartley, 2001). The Acronychia-Melicope clade also reaches
much higher altitudes compared to the Euodia clade, with
many species found above 3000 m in New Guinea, and M.
brassii to 4275 m (Hartley, 2001). Adaptations to a wider
ecological range might partly explain the higher species
richness in the Acronychia-Medicosma-Melicope clade.
Species of the Euodia clade and the Acronychia-Melicope
clade are similar in many morphological characters including
habit, leaf morphology, indumentum, and ower morphol-
ogy (Hartley, 2001; Kubitzki et al., 2011). The main differences
between the two clades are in fruit types, presentation
of seeds and seed coat anatomy. Several genera of the
Acronychia-Melicope clade have drupaceous fruits, while
most (including Melicope) have dehiscent fruits in which
the ripe seeds remain attached upon dehiscence and are
thereby displayed to potential seed dispersers. In contrast,
species of the Euodia clade (except the drupaceous
Pitaviaster haplophyllus (F.Muell.) T.G.Hartley) have follicular
fruits in which seeds are elastically discharged with the
endocarp when the fruit opens (Hartley, 2001, 2013). The
seeds of the Euodia clade have a thin and brittle testa without
the shiny pellicle (Hartley, 2001; Kubitzki et al., 2011). Seeds of
the Acronychia-Melicope clade have a thick sclerotesta, a
spongy nutritious sarcotesta, and a shiny black pellicle;
features that have been interpreted as adaptations for bird
dispersals, with the spongy sarcotesta as the nutrient layer,
the shiny pellicle as visual attractant, and the sclerotesta to
protect the embryo from digestion (Hartley, 2001). The
visibility of the seeds in the open fruits is further enhanced by
a colorful and eshy exocarp in some Melicope species
(Hartley, 2001). Field observations conrm that birds act as
seed dispersers for Acronychia and Melicope (Frith et al., 1976;
Floyd, 1989; Innis, 1989; Hartley, 2001; Medeiros, 2004). On
the Hawaiian Islands, where 71% of the native bird species
have become extinct (Aslan et al., 2013), Melicope seeds are
dispersed by two invasive bird species (Medeiros, 2004;
Foster & Robinson, 2007). Bird-dispersal has been postulated
for many taxa, especially for the colonization of the Hawaiian
Islands and other isolated oceanic islands (Carlquist, 1967;
Sakai et al., 1995; Foster & Robinson, 2007; Keeley & Funk,
2011; Aslan et al., 2013; Roy et al., 2013).
While several morphological traits seem obvious adapta-
tions to bird dispersal, it is impossible to exclude additional
dispersal vectors of primarily bird-dispersed species (Wenny
et al., 2016). Since LDD events are generally rare and unusual,
the standard dispersal vector(s) might not account for LDD.
Instead, either an unusual behavior of the standard vector
(e.g., a vagrant in the case of ornithochory) or a different
vector might have caused a LDD event (Higgins et al., 2003;
Nathan et al., 2008). It is premature to accept adaptations to
bird dispersal as the sole factor to explain the differences in
distribution and species richness between the Acronychia-
Melicope and Euodia groups. Nevertheless, bird-dispersal
might have played a crucial role especially in island systems
such as the Malesian region and/or within the Hawaiian
Islands.
Acknowledgements
We thank the numerous individuals (F. Brambach, B.
Chantarasuwan, H.-J. Esser, T. Hartley, S. James, D. Lorence,
H. Oppenheimer, P. Pelser, S. Perlman, S. Razamandimbison,
M. Rossetto, Y. Sirichamorn, G. Weiblen, W. de Wilde, B. de
Wilde-Duyfjes, K. Wood, and Z. Zhou) and institutions
(Herbaria A, C, CANB, L, LAE, MO, NY, P, PTBG, QRS, SNP;
Australian National Botanic Garden, Hortus Botanicus Leiden,
National Tropical Botanical Garden, Southern Cross Univer-
sity) for providing samples for this study, J. Kr
uger (GOET) for
lab assistance, and A.J. Harris for assistance with MrBayes via
the use of the Oklahoma State University High Performance
Computing Center Resources.
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Supplementary Material
The following supplementary material is available online
for this article at http://onlinelibrary.wiley.com/doi/10.1111/jse.
12299/suppinfo:
Fig. S1. Phylogenetic reconstruction of the Acronychia-Euodia-
Melicope clade using Bayesian inference. The 50% majority-rule
consensus tree of the MrBayes analysis is shown with
posterior probability (pp) values above the branches.
24 Appelhans et al.
J. Syst. Evol. 9999 (9999): 1–24, 2018 www.jse.ac.cn
... Past cladistic analyses involving Boronia fall into three main groups: (1) subfamilial studies that included many genera but understandably only a few representatives from each genus (Scott & al., 2000;Groppo & al., 2008Groppo & al., , 2012Bayly & al., 2013;Appelhans & al., 2014aAppelhans & al., , 2018Appelhans & Wen, 2020); (2) analyses of a good representation of the genus Boronia but with a small number of outgroups (Weston & al., 1984;Shan & al., 2006;Duretto & al., in prep.); or (3) studies investigating species groups (Burgman, 1985) or a specific section of Boronia (Duretto & Ladiges, 1999;Duretto, 2003). ...
... In previous subfamilial studies, Boronia was represented by only one species in Scott & al. (2000; from section Pedunculatae), Groppo & al. (2008Groppo & al. ( , 2012 section Boronia), Appelhans & al. (2014aAppelhans & al. ( , 2018 section Boronella), and Appelhans & Wen (2020; section Boronia) and four species in Bayly & al. (2013; two species from section Boronella, one species from section Valvatae, and B. scabra Lindl., which is currently placed incertae sedis). These studies did not include a representative sample of the diversity found in Boronia, with sections Alatae, Algidae, Cyanothamnus and Imbricatae never being included in a study of this type. ...
... In this paper we aim to test the monophyly of Boronia by including representatives of all sections and most series of the genus, plus a large number of genera representing the Australasian-Malesian clades identified by Groppo & al. (2008), Bayly & al. (2013: clade A), Appelhans & al. (2014aAppelhans & al. ( , 2018 and Morton & Telmer (2014) in which Boronia is placed. ...
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The monophyly of Boronia (Rutaceae) was tested using 134 accessions of 120 species belonging to 39 genera from subfamily Amyridoideae. Taxa included representatives of all eight sections of Boronia plus species of most genera in the two main clades related to Boronia that had been identified by earlier studies. These samples included a good representation of genera from both rainforest and sclerophyllous biomes. Maximum parsimony and Bayesian inference analyses were performed using three plastid markers (psbA‐trnH, trnL‐trnF, rbcL) and two nuclear ribosomal markers (ITS, ETS). Separate analyses of plastid and nuclear sequences using either maximum parsimony or Bayesian inference analyses recovered similar topologies. Apart from Boronia, the broad generic relationships of previous analyses were largely supported. Boronia is polyphyletic with section Cyanothamnus being more closely related to a large clade containing genera found in rainforest, including Melicope, Acronychia and their relatives. The remaining seven sections of Boronia formed a strongly supported and isolated group. Boronia sensu stricto is sister to a clade containing the Cyanothamnus‐Melicope‐Acronychia clade plus a clade containing Euodia, Zieria and other small genera found in rainforest or sclerophyllous communities. Issues with circumscriptions of ingroups and outgroups for previous analyses of Boronia and the complex relationship between Australasian genera found in rainforest and sclerophyllous communities are both discussed. Cyanothamnus is reinstated at generic level. Appropriate nomenclatural changes are made to transfer all currently recognised series, species, subspecies and varieties of Boronia sect. Cyanothamnus to the genus Cyanothamnus.
... The genus Melicope J.R. Forst. and G. Forst. is a member of the Rutaceae (Rue or Citrus family) and contains circa 239 species distributed in the Malagasy, Indo-Himalayan, South-East Asian, and Pacific regions [1,2]. With 54 currently accepted endemic species on the Hawaiian Islands, Melicope ranks among the three most speciose lineages of the archipelago [3,4]. ...
... However, some new Hawaiian species have recently been discovered and botanically described [6][7][8]. Melicope has been subdivided into four sections based on morphology, and molecular phylogenetic studies have demonstrated that only one of them is monophyletic [1,2]. All Hawaiian species belong to section Pelea. ...
... All steps were performed under argon stream to avoid oxidation. 1 ...
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The dichloromethane extract from leaves of Melicope barbigera (Rutaceae), endemic to the Hawaiian island of Kaua’i, yielded four new and three previously known acetophenones and 2H-chromenes, all found for the first time in M. barbigera. The structures of the new compounds obtained from the dichloromethane extract after purification by chromatographic methods were unambiguously elucidated by spectroscopic analyses including 1D/2D NMR spectroscopy and HRESIMS. The absolute configuration was determined by modified Mosher’s method. Compounds 2, 4 and the mixture of 6 and 7 exhibited moderate cytotoxic activities against the human ovarian cancer cell line A2780 with IC50 values of 30.0 and 75.7 µM for 2 and 4, respectively, in a nuclear shrinkage cytotoxicity assay.
... Several studies have extensively sampled taxa from both island and continental lineages and included sufficient molecular data to resolve deep divergences with statistical power. A number of Hawaiian groups are now known to have successfully colonized other remote archipelagos or even continents, including Hawaiian Drosophilidae (O'Grady and DeSalle 2008;O'Grady et al. 2011;Lapoint et al. 2013), sandalwoods (Harbaugh and Baldwin 2007), Melicope (Appelhans et al. 2014(Appelhans et al. , 2018, snails (Rundell et al. 2004), potentially other plant groups (Price and Wagner 2018), and possibly even birds (Filardi and Moyle 2005). There is ample evidence of biotic exchange between remote archipelagos across the Pacific and Indian Oceans (Cibois et al. 2011;Hembry et al. 2013;Le Roux et al. 2014;Andersen et al. 2015), suggesting that the Hawaiian Islands are more likely part of a broader global exchange of species than a turgid backwater. ...
... Interestingly, members of the genus Scaptomyza seem to have escaped from Hawaiʻi during approximately the last 15 million years and gone on to colonize several continental landmasses (O'Grady and DeSalle 2008;Lapoint et al. 2013). This island-to-continent biogeographic pattern is unique among insects, although has been observed in plant and snail lineages (Rundell et al. 2004;Harbaugh and Baldwin 2007;Appelhans et al. 2014Appelhans et al. , 2018. ...
... This result is not surprising considering the isolation of the Hawaiian archipelago. For many angiosperm genera, the Hawaiian diversity has been shown to result from a single colonization event, for example, in Psychotria (Nepokroeff et al. 1999), Silene (Eggens et al. 2007), the lobeliads (Givnish et al. 2009), the Stachydeae (Roy et al. 2015;Welch et al. 2016; the Hawaiian lineage being embedded in the genus Stachys), Melicope (Appelhans et al. 2018), and Myrsine (Appelhans et al. 2020). In ferns and lycophytes, however, the pattern appears to be different due to their generally higher dispersal capacities. ...
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The Hawaiian Islands are an emblematic field to study evolution, with their very high rates of endemism and spectacular cases of insular speciation. Nevertheless, many Hawaiian lineages still deserve investigation, such as in the fern lineage. In this study, we address the question of the origin of the fern genus Ctenitis, which is present in the archipelago with two endemic species, Ctenitis squamigera and C. latifrons. Using a taxonomic sampling covering the pan-tropical distribution of the genus and three chloroplast DNA regions, we provide evidence that the genus in the Hawaiian Islands originated from a single long-distance dispersal from the Neotropics. This area is less represented than Asia and the South Pacific in the origin of Hawaiian ferns, but a Neotropical origin may be explained by the transportation of spores by tropical storms originating near Central America. Furthermore, the colonization of the Hawaiian Islands is estimated to have occurred between 4 [9-2] and 3 [7-1] mya. This timing is consistent with the ages of all main and extant islands of the archipelago, which already provided habitats for the establishment of the initial Ctenitis colonizer. In turn, this relatively late arrival to the islands and the related potentially low availability of ecological niches may have hampered diversification of the genus beyond the two extant species. ARTICLE HISTORY
... There have been four recent studies that aimed at resolving broader relationships in the species-rich genus Melicope and its relatives and in the diverse group of Australasian Rutaceae (Bayly & al., 2013;Appelhans & al., 2014Appelhans & al., , 2018bDuretto & al., 2020). Our study improved the support and resolution of several nodes in the backbone of this clade, and it agrees with these three previous studies that Boronia and Melicope are both polyphyletic in their traditional circumscriptions. ...
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Rutaceae is a family of angiosperms well known for the economically important genus Citrus. The division of Rutaceae into subfamilies is still inadequate and provisional. Previous phylogenetic studies at the family level are characterized by a limited sampling of genera and lack several crucial taxa. Here, we present a phylogenetic study based on six nuclear and plastid markers including 87.7% of the currently accepted genera, which is more than twice as many as in previous studies. Seven genera are included in a phylogenetic analysis for the first time. Most clades are resolved with high support, and we propose a new subfamily classification for Rutaceae that comprises the subfamilies Amyridoideae, Aurantioideae, Cneoroideae, Haplophylloideae, Rutoideae and Zanthoxyloideae. Aurantioideae is the only traditional subfamily that is resolved as monophyletic. We tested whether 13 morphological and karyological characters are taxonomically informative in Rutaceae. Chromosome numbers are clearly different in the two main clades of Rutaceae, but fruit characteristics, which have been used to define subfamilies in the past, do not distinguish between the main lineages of the family.
... In this volume, articulated the famous progression rule for hotspot archipelagos: clades tend to inhabit older islands first and disperse to younger islands in the order that the islands appear. The large collection of papers in set the foundation for phylogenetic biogeographic research and inspired numerous subsequent studies on the Hawaiian archipelago, the Pacific, and island systems in general (Appelhans et al., 2018a(Appelhans et al., , 2018b. On our expedition to Tibet in 2006 (Fig. 4), Vicki often discussed with the many young participants on the island-like systems on the vast Qinghai-Tibetan Plateau in Asia and inspired many phylogenetic biogeographic studies in that region (e.g., Baird et al., 2010;Wen et al., 2013Wen et al., , 2014Nie et al., 2013Nie et al., , 2016Zhang et al., 2019). ...
Article
This special issue honors Dr. Vicki Ann Funk (26 November 1947 – 22 October 2019), who passed away after a battle with an aggressive cancer (Fig. 1). Dr. Funk was a Botanist at the Smithsonian Institution in 1981–2019. This article is protected by copyright. All rights reserved.
... & G. Forst. (Rutaceae), for which molecular dating suggested an age older than that of the current high islands (Givnish et al., 2009;Appelhans et al., 2018). ...
Article
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The Hawaiian radiation of Myrsine (primrose family, Primulaceae) is the only one among the ten most species‐rich Hawaiian plant lineages that has never been included in a phylogenetic analysis. Our study is based on a RADseq dataset of nearly all Hawaiian Myrsine species and a Sanger sequencing dataset based on a worldwide sampling of Myrsine and related genera. Myrsine as a whole might be paraphyletic with respect to the monotypic Macaronesian genera Heberdenia and Pleiomeris , while Hawaiian Myrsine is resolved as monophyletic. The Sanger sequencing proved to be insufficient to resolve the Hawaiian lineage, while RADseq fully resolved the relationships with high support. Hawaiian Myrsine consists of three main lineages, one of which contains the majority of species and is mainly confined to Kauaʻi, while the other two lineages primarily consist of few widespread species. While phylogenetic reconstructions delivered fully resolved and supported tree topologies, Quartet Sampling and HyDe analyses reveal phylogenetic incongruence throughout the phylogeny and provide the first molecular evidence of extensive hybridization in the lineage. This article is protected by copyright. All rights reserved.
... Aside from acting as a corridor for floristic exchanges among Africa, Eurasia, and Oceania, Madagascar is also a source of lineage diversification, such as the 12 genera of Celastraceae endemic to Madagascar (Bacon et al., 2016). Moleculardating analyses have demonstrated a recent colonization of Madagascar, with LDD considered as an important mechanism rather than the vicariance of the Gondwanan break-up (Buerki et al., 2013;Janssens et al., 2016;Appelhans et al., 2018;Appelhans & Wen, 2020). The only species in Madagascar (C. ...
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The mechanisms underlying the origin, evolution and distributional patterns of organisms are a major focus of biogeography. Vicariance and long‐distance dispersal (LDD) are two important explanations for disjunct distribution patterns among lineages. In‐depth biogeographic studies of taxa that exhibit wide‐ranging disjunctions can provide valuable information for addressing the relative importance of these biogeographic mechanisms. The genus Celastrus contains ca. 30 species that are disjunctly distributed in five continents of both Northern and Southern Hemisphere, providing an excellent system for historical biogeographic analyses. Here, we used sequence data from five markers (nuclear ETS and ITS, and plastid psbA‐trnH , rpl16 and trnL‐F ) to reconstruct the phylogeny of Celastrus and investigate its phylogenetic relationships with Tripterygium , estimate clade divergence times using the fossil‐calibrated method, and infer its ancestral distribution range. Celastrus and Tripterygium were each supported as monophyletic. The morphology‐based classification systems were not supported by the phylogenetic results. The divergence time between Celastrus and Tripterygium was estimated to be 26.22 Ma (95% HPD: 24.46–28.17 Ma), and the diversification of Celastrus were suggested to be linked to global warming events during the Miocene. Celastrus was suggested to have a tropical Asian origin, and dispersed to Central and South America, North America, Oceania, and Madagascar at different period, most probably through LDD. Birds may have facilitated transoceanic migrations of Celastrus because of its bi‐colored fruits, which contain red and fleshy arils. Our results highlight the importance of key morphological innovations and animal‐mediated dispersals for the rapid diversification of plant lineages across vast distributional ranges. This article is protected by copyright. All rights reserved.
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Seed dormancy varies greatly between species, clades, communities, and regions. We propose that fireprone ecosystems create ideal conditions for the selection of seed dormancy as fire provides a mechanism for dormancy release and postfire conditions are optimal for germination. Thus, fire‐released seed dormancy should vary in type and abundance under different fire regimes. To test these predictions, we compiled data from a wide range of fire‐related germination experiments for species in different ecosystems across the globe. We identified four dormancy syndromes: heat‐released (physical) dormancy, smoke‐released (physiological) dormancy, non‐fire‐released dormancy, and non‐dormancy. In fireprone ecosystems, fire, in the form of heat and/or chemical by‐products (collectively termed ‘smoke’), are the predominant stimuli for dormancy release and subsequent germination, with climate (cold or warm stratification) and light sometimes playing important secondary roles. Fire (heat or smoke)‐released dormancy is best expressed where woody vegetation is dense and fires are intense, i.e. in crown‐fire ecosystems. In such environments, seed dormancy allows shade‐intolerant species to take advantage of vegetation gaps created by fire and synchronize germination with optimal recruitment conditions. In grassy fireprone ecosystems (e.g. savannas), where fires are less intense but more frequent, seed dormancy is less common and dormancy release is often not directly related to fire (non‐fire‐released dormancy). Rates of germination, whether controls or postfire, are twice as fast in savannas than in mediterranean ecosystems. Fire‐released dormancy is rare to absent in arid ecosystems and rainforests. The seeds of many species with fire‐released dormancy also possess elaiosomes that promote ant dispersal. Burial by ants increases insulation of seeds from fires and places them in a suitable location for fire‐released dormancy. The distribution of these dormancy syndromes across seed plants is not random – certain dormancy types are associated with particular lineages (phylogenetic conservatism). Heat‐released dormancy can be traced back to fireprone floras in the ‘fiery’ mid‐Cretaceous, followed by smoke‐released dormancy, with loss of fire‐related dormancy among recent events associated with the advent of open savannas and non‐fireprone habitats. Anthropogenic influences are now modifying dormancy‐release mechanisms, usually decreasing the role of fire as exaptive effects. We conclude that contrasting fire regimes are a key driver of the evolution and maintenance of diverse seed dormancy types in many of the world's natural ecosystems.
Article
Background There are conflicting views between palaeobotanists and plant systematists/evolutionary biologists regarding the occurrence of plant speciation in the Quaternary. Palaeobotanists advocate that Quaternary speciation was rare despite opposing molecular phylogenetic evidence, the extent of which appears underappreciated. Aims To document, describe and discuss evidence for Quaternary plant speciation across different geographical regions based on dated molecular phylogenies and related studies. Methods From a search of the literature we compiled a selection mainly of dated molecular phylogenies from all continents (except Antarctica) and from all major climate zones. Results Molecular phylogenetic analyses and related studies show that Quaternary plant speciation and radiations occurred frequently and that in many instances Quaternary climatic oscillations were likely important drivers of them. In all geographical regions studied Quaternary plant speciation and radiations were particularly evident in mountainous areas and arid regions, and were also prevalent on all major oceanic archipelagos. Conclusions Based on our survey of the molecular phylogenetic and related literature we propose there is now overwhelming evidence that plant speciation and radiations were ubiquitous during the Quaternary. We therefore reject the view of palaeobotanists that plant speciation was rare during this period and briefly discuss possible reasons for this discrepancy.
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Platydesma, an endemic genus to the Hawaiian Islands containing four species, has long been considered of obscure origin. Recent molecular phylogenetic studies have unequivocally placed Platydesma within the widespread genus Melicope as sister to the rest of the Hawaiian species of Melicope. This makes submerging Platydesma into Melicope necessary. We make the necessary new combinations: Melicope cornuta (Hillebr.) Appelhans, K.R. Wood & W.L. Wagner, M. cornuta var. decurrens (B.C.Stone) Appelhans, K.R. Wood & W.L. Wagner, M. remyi (Sherff) Appelhans, K.R. Wood & W.L. Wagner, and M. rostrata (Hillebr.) Appelhans, K.R. Wood & W.L. Wagner. An additional species that has been recognized within Platydesma should now be recognized under its original name M. spathulata A. Gray. All Hawaiian species belong to Melicope section Pelea. Our molecular phylogenetic studies also showed that in addition to merging Platydesma into section Pelea, five species described from New Caledonia need to be excluded from the section in order to achieve monophyly of section Pelea.
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Melicope stonei K.R. Wood, Appelhans & W.L. Wagner (section Pelea, Rutaceae), a new endemic tree species from Kaua'i, Hawaiian Islands, is described and illustrated with notes on its distribution, ecology, conservation status, and phylogenetic placement. The new species differs from its Hawaiian congeners by its unique combination of distinct carpels and ramiflorous inflorescences arising on stems below the leaves; plants monoecious; leaf blades (5-)8-30 × (4-)6-11 cm, with abaxial surface densely tomentose, especially along midribs; and very long petioles of up to 9 cm. Since its discovery in 1988, 94 individuals have been documented and are confined to a 1.5 km²69 region of unique high canopy mesic forest. Melicope stonei represents a new Critically Endangered (CR) single island endemic species on Kaua'i.
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This study focuses on reconstructing the time-calibrated phylogeny of the nine families comprising the order Sapindales, representing a diverse and economically important group of eudicots including citrus, mahogany, tree-of-heaven, cashew, mango, pistachio, frankincense, myrrh, lychee, rambutan, maple, and buckeye. We sampled three molecular markers, plastid genes rbcL and atpB, and the trnL-trnLF spacer region, and covered one-third of the generic diversity of Sapindales. All three markers produced congruent phylogenies using maximum likelihood and Bayesian methods for a set of taxa that included outgroups, i.e., members of the closely related orders Brassicales and Malvales, and the more distantly related Crossosomatales, Ranunculales, and Ceratophyllales. All results confirmed the current delimitation of the families within Sapindales, and the monophyly of the order. Concerning inter-familial relationships, Biebersteiniaceae and Nitrariaceae formed a basal grade (or sister clade) to the rest of Sapindales with moderate support. The sister relationship of Kirkiaceae to Anacardiaceae and Burseraceae was strongly supported. The clade combining Anacardiaceae and Burseraceae as well as the clade combining Meliaceae, Simaroubaceae, and Rutaceae each received strong support. The sister relationship between Meliaceae and Simaroubaceae was moderately supported. The position of Sapindaceae could not be resolved with confidence. The Sapindales separated from their sister clade, comprising Brassicales and Malvales, in the Early Cretaceous at ca. 112 Ma, and diversified into the nine families from ca. 105 Ma until ca. 87 Ma during Early to Late Cretaceous times. Biebersteiniaceae and Nitrariaceae have the longest stem lineages observed in Sapindales, possibly indicating that extinction may have had a greater role in shaping their extant diversity than elsewhere within the order. Divergence within the larger families (Anacardiaceae, Burseraceae, Meliaceae, Rutaceae, Sapindaceae, Simaroubaceae) started during the Late Cretaceous, extending into the Paleogene and Neogene. © 2016, International Association for Plant Taxonomy. All rights reserved.
Article
Plastid (trnL intron and trnL-F spacer) and nuclear (ITS-1 and ITS-2 rDNA) regions were analyzed to infer the phylogeny and evaluate the classification of Rutaceae subfamilies Rutoideae and Toddalioideae. The inferred phylogeny lends support to merging these two subfamilies established by Engler based on different fruit types. Moreover, Phellodendron, Tetradium, Toddalia, and Zanthoxylum were resolved as a clade, supporting the proposal for a 'proto-Rutaceae' group. The molecular data also showed that members of Euodia sensu lato should be placed in three different genera: Tetradium, Euodia, and Melicope. The latter two genera are more closely related to Acronychia than they are to Tetradium. Except for the discrepancy in the position of Melicope vitiflora, the cladistic results are congruent with the morphological and biochemical interpretations made by two previous authors.