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A molecular phylogeny of Southeast Asian Cyrtandra (Gesneriaceae) supports an emerging paradigm for Malesian plant biogeography

Authors:
  • DKI US Pacific Basin Agricultural Research Center USDA-ARS
  • National Research and Innovation Agency

Abstract and Figures

The islands of Southeast Asia comprise one of the most geologically and biogeographically complex areas in the world and are a centre of exceptional floristic diversity, harbouring 45,000 species of flowering plants. Cyrtandra, with over 800 species of herbs and shrubs, is the largest genus in the family Gesneriaceae and is one of the most emblematic and species-rich genera of the Malesian rainforest understorey. The high number of species and tendency to narrow endemism make Cyrtandra an ideal genus for examining biogeographic patterns. We sampled 128 Cyrtandra taxa from key localities across Southeast Asia to evaluate the geo-temporal patterns and evolutionary dynamics of this clade. One nuclear and four chloroplast regions were used for phylogenetic reconstruction, molecular dating, and ancestral range estimation. Results from the dating analysis suggest that the great diversity of Cyrtandra seen in the Malesian region results from a recent radiation, with most speciation taking place in the last five million years. Borneo was recovered as the most likely ancestral range of the genus, with the current distribution of species resulting from a west to east migration across Malesia that corresponds with island emergence and mountain building. Lastly, our investigation into the biogeographic history of the genus indicates high levels of floristic exchange between the islands on the Sunda shelf and the important role of the Philippines as a stepping stone to Wallacea and New Guinea. These patterns underlie much of the plant diversity in the region and form an emerging paradigm in Southeast Asian plant biogeography.
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Frontiers of Biogeography
Title
A molecular phylogeny of Southeast Asian Cyrtandra (Gesneriaceae) supports an
emerging paradigm for Malesian plant biogeography
Permalink
https://escholarship.org/uc/item/8h1560m6
Journal
Frontiers of Biogeography, 12(1)
Authors
Atkins, Hannah J.
Bramley, Gemma L.C.
Johnson, Melissa A.
et al.
Publication Date
2020
DOI
10.21425/F5FBG44184
Supplemental Material
https://escholarship.org/uc/item/8h1560m6#supplemental
License
https://creativecommons.org/licenses/by/4.0/ 4.0
Peer reviewed
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Frontiers of Biogeography
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ReseaRch aRticle
© the authors, CC-BY 4.0 license 1
Frontiers of Biogeography 2020, 12.1, e44814
e-ISSN: 1948-6596 https://escholarship.org/uc/fb doi:10.21425/F5FBG44814
a
A molecular phylogeny of Southeast Asian Cyrtandra (Gesneriaceae)
supports an emerging paradigm for Malesian plant biogeography
Hannah J. Atkins1*, Gemma L.C. Bramley2, Melissa A. Johnson3,
Abdulrokhman Kartonegoro4, Kanae Nishii1,5, Goro Kokubugata6,
Michael Möller1 and Mark Hughes1
1 Royal Botanic Garden Edinburgh, 20a Inverleith Row, Edinburgh, EH3 5LR, Scotland, UK; 2 Royal Botanic Gardens, Kew,
Richmond, Surrey, TW9 3AE, UK; 3USDA Agricultural Research Service, DKI US Pacic Basin Agricultural Research Center,
64 Nowelo St., Hilo, HI, USA; 4 Research Center for Biology, Indonesian Instute of Sciences (LIPI), Jl. Jakarta‑Bogor
KM. 46, Cibininong, West Java 16911, Indonesia;
5
Kanagawa University, 2946, Tsuchiya, Hiratsuka‑shi, Kanagawa,
Japan; 6 Department of Botany, Naonal Museum of Nature and Science, Amakubo Tsukuba, Ibaraki 305‑0005, Japan.
*Corresponding author: h.atkins@rbge.org.uk
Highlights
This paper provides the rst well sampled phylogeny
of Cyrtandra across Southeast Asia.
One of the richest genera of the Asian rainforest
understory, Cyrtandra appears to have originated in
Borneo, and undergone west‑to‑east dispersal into
the Pacic.
Support was found for a mid‑Miocene origin, with
most extant diversity arising by speciaon within the
last 5 Ma.
The Philippines appear to represent an important
secondary source area and stepping stone to Wallacea,
Taiwan and Japan, and New Guinea.
Cyrtandra fits into an emerging paradigm for
Southeast Asian plant geography, illustrang the role
of geo‑tectonic and climate processes in historical
biogeographical paerns in the region.
Abstract
The islands of Southeast Asia comprise one of the most
geologically and biogeographically complex areas in the
world and are a centre of exceponal orisc diversity,
harbouring 45,000 species of owering plants. Cyrtandra,
with over 800 species of herbs and shrubs, is the largest
genus in the family Gesneriaceae and is one of the most
emblemac and species‑rich genera of the Malesian
rainforest understorey. The high number of species
and tendency to narrow endemism make Cyrtandra
an ideal genus for examining biogeographic paerns.
We sampled 128 Cyrtandra taxa from key localies across
Southeast Asia to evaluate the geo‑temporal paerns
and evoluonary dynamics of this clade. One nuclear
and four chloroplast regions were used for phylogenec
reconstrucon, molecular dang, and ancestral range
esmaon. Results from the dang analysis suggest that
the great diversity of Cyrtandra seen in the Malesian region
results from a recent radiaon, with most speciaon
taking place in the last ve million years. Borneo was
recovered as the most likely ancestral range of the genus,
with the current distribuon of species resulng from a
west to east migraon across Malesia that corresponds
with island emergence and mountain building. Lastly,
our invesgaon into the biogeographic history of the
genus indicates high levels of orisc exchange between
the islands on the Sunda shelf and the important role
of the Philippines as a stepping stone to Wallacea and
New Guinea. These paerns underlie much of the plant
diversity in the region and form an emerging paradigm
in Southeast Asian plant biogeography.
Keywords: ancestral range esmaon, biogeographic stochasc mapping, Cyrtandra, orisc exchange, island biogeography,
molecular dang, recent divergence, Sahul shelf, Sunda shelf, Wallacea
Atkins et al.
Frontiers of Biogeography 2020, 12.1, e44814 © the authors, CC-BY 4.0 license 2
Molecular phylogeny of southeast Asian Cyrtandra
Introduction
The islands of Southeast Asia comprise one of the
most geologically and biogeographically complex areas
in the world (Hall 2002, Lohman et al. 2011) and are
the meeng and mixing point of oras and faunas of
diverse origins (van Welzen et al. 2011, Richardson et al.
2012). The area is esmated to harbour approximately
45,000 species of vascular plants (Johns 1995) on more
than 20,000 islands (Lohman et al. 2011). It contains the
biodiversity hotspots of Sundaland, Wallacea and the
Philippines (Brooks et al. 2006), and the mega‑diverse
island of New Guinea (Miermeier et al. 2003, Takeuchi
2005, Hoover et al. 2017).
The Malesian region is a complex and intricate
mosaic of islands of dierent origins with a dynamic
history over the last 50 million years (Ma) (Hall 2002,
2012a,b). In the west of the region are the connental
Sunda shelf islands of Sumatra, Java and Borneo,
separated by shallow seas. In the centre are the
numerous smaller terranes and oceanic islands that
comprise the Philippines and Wallacea, and in the east
is the Sahul shelf and the large island of New Guinea,
which is itself of composite origin. Adding a layer
of complexity to this is the changing climate of the
past 50 ma (Morley 2012, 2018), most strikingly the
uctuang glacials and interglacials of the Pleistocene
(Woodru 2010, Morley 2012), which impacted sea
levels and the extent of vegetaon types (Woodru
2010, Cannon 2012, Morley 2012).
Over the last decade, a number of dated molecular
phylogenies (Thomas et al. 2012, Grudinski et al.
2014, Hughes et al. 2015, Williams et al. 2017) and
meta‑analyses (van Welzen et al. 2011, De Bruyn et al.
2014, Crayn et al. 2015) have supplemented our knowledge
of how current paerns of diversity have been shaped
by the geological and climac history of Malesia. These
studies have provided insights into where and when
lineages diversied and revealed some remarkable
cross‑taxon biogeographic paerns (Lohman et al.
2011), including the predominance of west‑to‑east
dispersal paerns (Su and Saunders 2009, Baker and
Couvreur 2012, Richardson et al. 2012, Thomas et al.
2012, Grudinski et al. 2014, Richardson et al. 2014,
Crayn et al. 2015) and the idencaon of Borneo as
an ancestral area and centre of diversity. Our current
understanding of the biogeographic history of Malesia,
however, remains incomplete and there is a need
for addional well sampled phylogenies of taxa with
distribuons across the region (Richardson et al. 2012,
Webb and Ree 2012).
Cyrtandra is the largest genus in the Gesneriaceae,
with over 800 species of herbs and shrubs (Atkins et al.
2013) and is a key component of the herbaceous
layer of Malesian rainforest found from sea level to
3000m (Bur 2001, Atkins et al. 2013). Centres of
diversity for the genus in Southeast Asia are Borneo
(~200 spp.), the Philippines (~150 spp.), and New
Guinea (~120 spp.) (Atkins et al. 2013). Its high species
diversity, large number of narrow endemic species,
and wide distribuon make it an ideal genus for
examining biogeographic paerns (Atkins et al. 2001,
Cronk et al. 2005, Clark et al. 2008, Johnson et al.
2017) and invesgang the processes which underlie
current paerns of biodiversity (Bramley et al. 2004a,
Johnson et al. 2015, 2019). The genus is characterised
by a combinaon of two ferle stamens and an
indehiscent fruit, which varies from a tough‑walled
green or brown capsule in the west to a eshy berry
that ripens white or rarely orange in the east of its
distribuon, parcularly in New Guinea and the Pacic
(Fig. 1) (Clark et al. 2013, Johnson 2017, Atkins et al.
Figure 1. Range of fruit morphology in SE Asian and Pacic Cyrtandra. a C. pendula (Sumatra) SUBOE 2; b C. sp (Sumatra)
SUBOE 6; c C. sp (Sumatra) SUBOE 9; d C. sp (New Guinea) Briggs MB838; e C. pogonantha (Samoa) Wood 16941 f
C. celebica (Sulawesi) BAKK 12; g C. polyneura (Sulawesi) BAKK 18; h C. pulleana (New Guinea) Briggs MB845; I C. richii
(Samoa) Wood 16935. Photos: a‑c, f & g: Sadie Barber. e & i: Melissa Johnson. d & h: Marie Briggs.
Atkins et al.
Frontiers of Biogeography 2020, 12.1, e44814 © the authors, CC-BY 4.0 license 3
Molecular phylogeny of southeast Asian Cyrtandra
2019). The owers are oen white but species with
pink, red, purple, yellow, green, and orange owers
are also known (Fig. 2).
Earlier phylogenec studies of Southeast Asian
Cyrtandra have focused on parcular localies with
dense sampling from a small number of locaons
(Atkins et al. 2001, Bramley et al. 2004a). Larger scale
studies have focused on Cyrtandra diversicaon
across the Pacic (Cronk et al. 2005, Clark et al. 2008,
2009, Johnson et al. 2017), and these studies have
signalled that the origin of the genus is within the
Malesian region. Here, we sample Cyrtandra taxa
from key localies across Southeast Asia to construct
a well‑resolved phylogenec tree based on one
nuclear and four chloroplast regions. We use this
to esmate divergence mes, ancestral ranges, and
dispersal paerns in order to gain insights into the
evoluonary history of Cyrtandra. We then consider
whether the key paerns recovered for other taxa
in Southeast Asia are also seen in Cyrtandra, one of
the most species‑rich and emblemac genera of the
Malesian rainforest understorey.
Methods
Taxon sampling
We sampled a total of 192 accessions represenng
128 Cyrtandra taxa (Supplementary Table S1),
including samples that were representave of all the
key regions in Southeast Asia (Fig. 3). Table 1 gives a
summary of our sampling against current esmates
of species numbers by island for the Southeast Asian
region (Atkins et al. 2013). Five taxa from within
Didymocarpinae (the same subtribe as Cyrtandra) were
selected as outgroups (Aeschynanthus roseoorus,
A. buxifolius, Agalmyla chalmersii, Didymocarpus
anrrhinoides, and Loxosgma grithii). Outgroups
were selected to reect those in recent molecular
dang analyses (Johnson et al. 2017, Ranasinghe
2017) to facilitate dang of the nodes using secondary
calibraon points. We applied names to as many of
the samples as possible but many of the samples
represent undescribed diversity. There is no single
taxonomic treatment for Cyrtandra and therefore
species concepts and idencaons follow those
used in regional treatments (e.g., Atkins and Cronk,
2001, Bramley et al. 2004b).
Molecular methods
DNA extraction methods and PCR conditions
followed Nishii et al. (2019). Details of the primers
used for each of the five regions (ITS, matK,
trnL‑F, psbA-trnH and rpl32‑trnL) are given in
Table 2. Chloroplast sequence data (matK, trnL‑F,
psbA-trnH and rpl32‑trnL) from two of the outgroup
collections, Agalmyla chalmersii and Didymocarpus
antirrhinoides, was gifted to the project by Prof Gao
Lian Ming, Kunming Institute of Botany, Chinese
Academy of Sciences, Yunnan, China.
Phylogenetic analyses
Maximum Parsimony (MP) analyses were inially
conducted on individual regions to visually assess
Figure 2. Range of ower morphology in SE Asian Cyrtandra. a Cyrtandra rantemarioensis (Sulawesi) RBGE living collecons
20000622; b. Cyrtandra luteiora (Sulawesi) RBGE living collecons 20021194; c. Cyrtandra purpureofucata (Sulawesi)
Thomas & Ardi 09‑88; d. Cyrtandra serrafolia (Sulawesi) RBGE living collecons 20021210; e. Cyrtandra celebica (Sulawesi)
BAKK 15; f. Cyrtandra mollis (Sulawesi) BAKK 42; g. Cyrtandra cleopatrae (Palawan, Philippines) RBGE living collecons
19981745; h. Cyrtandra bungahijau (Yapen Island, New Guinea) RBGE living collecons 20090826; i. Cyrtandra peltata
(Sumatra) RBGE living collecon 20161282; j. Cyrtandra viata (Yapen Island, New Guinea) RBGE living collecon 20090734.
Photos: a & b: Steve Sco. c: Wisnu Ardi. d & g: Hannah Atkins. e, f & i: Sadie Barber. j: Lynsey Wilson
Atkins et al.
Frontiers of Biogeography 2020, 12.1, e44814 © the authors, CC-BY 4.0 license 4
Molecular phylogeny of southeast Asian Cyrtandra
congruence, with areas of conict determined by
examining the placement of individual taxa on each
gene tree. Relaonships were considered incongruent if
the placement of taxa varied among the individual gene
trees and exhibited MP‑BS values > 80%. MP analyses
were carried out using PAUP v 4.0a163 (Swoord 2002)
on unweighted and unordered characters. Alignment
gaps were treated as missing data. A heurisc search
was carried out using stepwise random addion of
10,000 replicates, with TBR and Multrees on. Stascal
Figure 3. Map showing collecon locaons of southeast Asian Cyrtandra samples included in the present study. Pacic
islands not shown on map.
Table 1. Current esmates of species numbers in Cyrtandra by area across Malesia, the number of species included in
the present study, and the percentage of the total that this represents.
Geographic region
(Southeast Asia only)
Total number of species
(following Atkins et al.
2013)
Number of species
sampled
% sampled (based on
maximum numbers
where ranges given in
Atkins et al. 2013)
Thailand 6 2 33
Peninsular Malaysia 9 5 56
Sumatra 40‑44 27 61
Java 19‑32 11 34
Lesser Sunda Islands 3 1 33
Borneo 181‑200 26 13
Taiwan and Japan 2 2 100
Philippines 105‑150 17 11
Sulawesi 22‑40 26 65
Moluccas 3 0 0
Australia 1 1 100
New Guinea 107‑120 10 8
Atkins et al.
Frontiers of Biogeography 2020, 12.1, e44814 © the authors, CC-BY 4.0 license 5
Molecular phylogeny of southeast Asian Cyrtandra
branch support was obtained from 10,000 heurisc
bootstrap replicates each starng with a random
addion tree, opmised with TBR on and Multrees
o. For Bayesian Inference and Maximum Likelihood
analyses, the data were divided into seven parons
(ITS spacers, 5.8S gene, psbA-trnH, rpl32‑trnL, trnL‑F,
matK coding region, matK intron region) and analysed
under the best‑t model of nucleode evoluon for
each genic region selected using the AIC criterion as
implemented in MrModeltest v 2.4 (Nylander 2004)
(GTR+G for ITS spacers, trnL‑F, psbA-trnH and matK
intron region, GTR+I+G for rpl32‑trnL and matK coding
region and SYM+I for the ITS 5.8S gene). Bayesian
inference (BI) phylogenec analyses were carried out
using Mr Bayes v 3.2.6 (Ronquist et al. 2012) on the
paroned dataset. Two runs with four chains each
were implemented, run for 10,000,000 generaons
with a tree sampled every 1000th generaon. The rst
10% of sampled trees were discarded as burn‑in and
the remainder summarised as a maximum clade
credibility tree and posterior probabilities (PP)
extracted. Maximum Likelihood (ML) analyses were
conducted with RAxML v 8 (Stamatakis 2014) via the
CIPRES Gateway (Miller et al. 2010). The search for
the opmal ML tree was performed with the ‘Let
RAxML halt bootstrapping automacally’ parameter
selected. For the ML and BI analyses, tree topology
and node support were examined in FigTree v. 1.4.3
(Rambaut 2007).
Divergence time estimates
A me‑calibrated phylogeny was constructed on the
paroned ve‑gene dataset using an uncorrelated
relaxed lognormal clock in the program BEAST v. 1.10.1
(Drummond et al. 2012, Rambaut et al. 2018). Secondary
age calibraons were necessary as there are no
unambiguous fossils in the Gesneriaceae family (Wiehler
1983, Clark et al. 2008). Five calibraon points were
taken from the family‑wide phylogeny in Ranasinghe
(2017) (Table 3) and were assigned a lognormal prior
following Ho and Phillips (2009) and Schenk (2016) .
Five separate runs were carried out, beginning with
a random tree and run for 100 million generaons
under a Yule model of speciaon, sampled every
1000 generaons. Following Condamine et al. (2015)
sensivity analyses using the Birth‑Death tree prior
were also run and the results were not signicantly
changed by choice of tree prior. The results from the
Table 2. Details of primers used for PCR and sequencing of the ve gene regions for Cyrtandra.
Region Name Direcon Primer sequences References
ITS ITS_5P Forward GGA AGG AGA AGT CGT AAC AAG Möller & Cronk 1997
ITS ITS_8P Reverse CAC GCT TCT CCA GAC TAC A Möller & Cronk 1997
trnLF trnLcG Forward GTG AAG ACT TCT AAA TTC AGA GAA AC Nishii et al. 2019
trnLF trnLf Reverse ATT TGA ACT GGT GAC ACG AG Taberlet et al. 1991
psbA‑trnHpsbAf Forward GTT ATG CAT GAA CGT AAT GCT C Sang et al. 1997
psbA‑trnH trnHr Reverse CGC GCA TGG TGG ATT CAC AAA TC Sang et al. 1997
rpl32‑trnLrpl32‑F Forward CAG TTC CAA AAA AAC GTA CTT C Shaw et al. 2007
rpl32‑trnL trnL(UAG) Reverse CTG CTT CCT AAG AGC AGC GT Shaw et al. 2007
matK matK.206F Forward CCG GGT TAT GAC AAT AAA TCC AGT Luna et al. 2019
matK matK.946R Reverse ATA AAT CCT TCT TGG ATG AAA CCA C Luna et al. 2019
matK matK.cy2F Forward TGG CAA TGG CAT TTT TCG CT Nishii et al. 2019
matK matK.1734R Reverse CCG TGC TTG CAT TTT TCA TTG C Luna et al. 2019
Table 3. Details of the ve secondary calibraon points (node age, standard deviaon, and prior distribuon) from
Ranasinghe (2017) used to generate the dated phylogeny of Cyrtandra in BEAST.
Calibraon
point Node Node Age
(Ma) Prior distribuon Standard
deviaon
1 Internal Cyrtandra node 6.42 LogNormal 2.0 (2.5, 10.97)
2Loxosgma and Cyrtandra crown 18.03 LogNormal 2.0 (14.18, 21.85)
3Aeschynanthus and Loxosgma/
Cyrtandra crown
18.79 LogNormal 2.0 (14.89, 22.71)
4Billolivia (and Aeschynanthus/
Loxosgma/ Cyrtandra crown
20.15 LogNormal 2.0 (16.18, 24.28)
5Agalmyla (and Billolivia/
Aeschynanthus/ Loxosgma/
Cyrtandra crown)
20.99 LogNormal 2.0 (17.04, 25.14)
Atkins et al.
Frontiers of Biogeography 2020, 12.1, e44814 © the authors, CC-BY 4.0 license 6
Molecular phylogeny of southeast Asian Cyrtandra
analysis with the Yule model are presented here. Plots
of the logged parameters for each run were visualised
using Tracer v. 1.7.1 (Drummond and Rambaut 2007)
to conrm convergence between runs by examining
log likelihood plots and ensuring that Eecve Sample
Size (ESS) values were above 200. The trees from
each run were combined in Logcombiner v 1.10.1
(Drummond et al. 2012) and support values and tree
stascs were summarised onto a single maximum
clade credibility (MCC) tree using the programme
TreeAnnotator v. 1.10.1 (Drummond et al. 2012),
visualised in FigTree v. 1.4.3 (Rambaut 2007).
Ancestral range estimation
The R package BioGeoBEARS (BioGeography with
Bayesian Evoluonary Analysis in R Scripts) (Matzke
2013, 2014) was used to esmate ancestral ranges
for Cyrtandra under three historical biogeography
methods: DEC (Dispersal‑Exncon‑Cladogenesis;
Ree and Smith, 2008), DIVA (Dispersal‑Vicariance
Analysis; Ronquist 1997), and BayArea (Bayesian
inference of historical biogeography for discrete areas;
Landis et al. 2013) models. Descripons of each of these
models and how BioGeoBEARS replicates their key
assumpons are given in Matzke (2013). To allow for
model comparison, all the models were implemented
in a maximum likelihood framework. As Cyrtandra is
distributed across a system of islands and shows high
levels of narrow endemism, founder event speciaon
was likely to be a highly relevant biogeographic process
(Cowie and Holland 2006, Matzke 2013, Roalson
and Roberts 2016, Johnson et al. 2017), so we also
explored the inuence of founder event speciaon in
the analysis by including ‘+J’ versions of the models.
Due to concerns about the stascal methods in the
package, both in terms of how the best t model is
selected and how the +J parameter operates (Ree and
Sanmarn 2018), results from all of the six models
will be discussed. Given that sampling density can
also impact the results, a summary of our sampling
rates against current species esmates is presented
in Table 1.
The MCC tree was pruned to include only a single
representave of each species except for those species
that have mul‑island distribuons and were not
monophylec, such as C. pendula. In these cases, we
included one representave from each area (following
Johnson et al. 2017, 2019). For monophylec species
with mul‑island distribuons, such as C. umbellifera
from Taiwan and the Philippines and C. sandei from
Java and Sumatra, only one sample was included, and
these were coded as present in each respecve area
in the analysis. Each taxon was assigned a distribuon
using 13 geographic regions based on a combinaon
of geological informaon (Hall 2002, 2012), previous
biogeographical studies (Atkins et al. 2001, van
Welzen et al. 2011, Hughes et al. 2015) and current
knowledge of species distribuons and relaonships in
Cyrtandra (Atkins and Cronk 2001, Bramley and Cronk
2003, Johnson et al. 2017, Kartonegoro et al. 2018).
The 13 regions used were: Hawaii, Marquesas and
Society Islands, Japan and Taiwan, Australia, Thailand,
Peninsular Malaysia, Sumatra, Borneo, Sulawesi, New
Guinea, Solomon Islands, Java and the Lesser Sunda
Islands, and the Philippines.
The outgroup taxa were removed so as not to
inuence the root ancestral area. We set the maximum
number of areas to two, as Cyrtandra is characterised by
high levels of narrow endemism and only C. pendula is
currently recognised as having a range size greater than
two areas. The six models (DEC, DIVA‑like, BayArea‑like,
and the ‘+J’ variaons of each) were compared for
stascal t using the Akaike Informaon Criterion
(AIC) and a Likelihood Rao Test (LRT).
Lastly, we used BioGeoBEARS to perform a
Biogeographic Stochasc Mapping (BSM) analysis
(Matzke 2016, Dupin et al. 2017). This generates
simulated histories based on a given biogeographical
model, the phylogeny, observed range data, and the
calculated ancestral state probabilies at each node
averaged over many realisaons. The biogeographical
events that are possible include within‑area speciaon,
vicariance and dispersal events (range expansions and
founder events). Event frequencies were esmated
by taking the mean of event counts from 100 BSMs.
We ran the BSM exercise on all the models to evaluate
the impact that the choice of model has on the event
counts.
Results
Phylogenetic relationships
In total, 940 new sequences were generated
for this study and our nal data matrix contained
ve gene regions and 5438 aligned base posions.
Tree topologies of independent MP analyses of the
ITS, trnL‑f, psbA‑trnH, rpl32, and matK regions were
congruent although there was far greater resoluon in
the ITS dataset than in any of the others individually.
The tree based on the concatenated ve‑gene dataset
(Fig. 4,5) largely followed the topology of the ITS tree,
with increased support for the relaonships between
the major clades. There were no incongruences with
greater than 80% MP bootstrap support. ML, MP, and
BI analyses of the combined dataset resulted in trees
with congruent topologies.
Divergence time estimates
In this study, divergence me esmates suggest
that the genus Cyrtandra split from its closest relave,
Loxosgma, c. 16 Ma (14.18‑18.34, 95% HPD) during
the early Miocene (Fig. 6). The crown age of Cyrtandra
is esmated to be 13 Ma (10.84‑15.56, 95% HPD).
Summaries of esmated dates are shown in Table 4.
Using mean ages, 109 of the 128 taxa included in the
analysis split from their most recent ancestor in the
last 5 ma (method following Madriñán et al. 2013;
Richardson et al. 2014).
Ancestral range estimation
Signicant improvement in the likelihood of the three
standard models (DEC, DIVA‑like, and BayArea‑like)
was seen when the founder event parameter (+J) was
added (Table 5). Of the six models evaluated, the best
t model was BayArea‑like +J.
Atkins et al.
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Molecular phylogeny of southeast Asian Cyrtandra
Table 4. Esmated ages (Ma) of major nodes (crown and stem age of Cyrtandra) in the present study using BEAST, and
comparable nodes in earlier studies. Ranges in parentheses represent the 95% highest posterior density (HPD).
Node Present study Johnson et al. 2017 Roalson and Roberts 2016
Cyrtandra stem 16.3 (14.28‑18.43) 25.27 (16.9‑35.02) 30.45 (14.79‑37.54)
Cyrtandra crown 13.38 (11.05‑15.79) 17.29 (12.54‑22.15) 11.08 (3.25‑21.78)
Table 5. Results of biogeographical model tesng in BioGeoBEARS for Cyrtandra. Model parameters include anagenec
dispersal (d), exncon (e), and jump dispersal or founder events (j). The best t model of BayAreaLike+J is highlighted
in bold.
Model LnL AIC AIC_wt # parameters d e J
DEC ‑258.8 521.7 1.80E‑21 2 0.0055 0.014 0
DEC+J ‑216 438 0.0027 3 0.0012 1.00E‑12 0.013
DIVALIKE ‑252.4 508.7 1.20E‑18 2 0.0058 1.00E‑12 0
DIVALIKE+J ‑218.3 442.6 0.0003 3 0.0014 1.00E‑12 0.013
BAYAREALIKE ‑280.4 564.8 8.00E‑31 2 0.0059 0.092 0
BAYAREALIKE+J -210.1 426.2 1 3 0.0005 0.0043 0.013
LnL = Log Likelihood, AIC = Akaike Informaon Criterion, AIC wt = AIC weight
Under all six models analysed, the island of Borneo
was recovered as the most likely ancestral area for
Cyrtandra (Fig. 7).
Biogeographic stochastic mapping
Under the best t model, Borneo is resolved as a
major source area with ~33% (11.5 events) of all dispersal
events originang here (Fig. 8, Table 6). Dispersal from
Borneo was most frequent to Sumatra (3.0 events) and
the Philippines (2.7 events), followed by Peninsular
Malaysia (2.0 events) and Sulawesi (1.5 events).
In contrast, Borneo was the recipient of only 0.8% of
dispersals from all other areas and no event counts
from any single area above 0.1. The Philippines was
the second largest source area with 21% of dispersal
events originang here. The majority of dispersal events
from the Philippines were to the island of Sulawesi
(3.9 events), but there were also dispersals from the
Philippines north to Taiwan and Japan (1.5 events)
and east to New Guinea (0.9 events). The greatest
source of dispersals into the Philippines was Borneo
(2.7 events). Relavely high levels of dispersal were
also recovered between Java, Sumatra, and Peninsular
Malaysia (2.5 events from Sumatra to Peninsular
Malaysia, 3.0 events from Java to Sumatra, and 1.2 events
from Sumatra to Java). In marked contrast to Borneo,
Sulawesi emerged as an island of high immigraon
(receiving 20% of all dispersals) and low emigraon,
with only 2% of dispersals originang here. New Guinea
is resolved as the most likely source of dispersals to
the Marquesas (0.9 events), Australia (1.0 event),
and the Solomon Islands (1.0 event). The stochasc
mapping exercise is more impacted by the choice of
model than the ancestral range esmaon as the six
models rely on dierent biogeographic processes.
In terms of dispersal paerns and potenal routes
through the region, however, Borneo is always in the
top three sources of dispersal in all the models, along
with the Philippines and Sumatra. Sulawesi is always
interpreted as being a poor source of dispersals under
all models. The Philippines is the most important
source of dispersals north to Taiwan and Japan under
all models. It is the highest source of dispersals south
to Sulawesi in all but the two worst t models where it
is the second highest aer Borneo; and it is the highest
source of dispersals east to New Guinea in all but the
two worst t models where Sumatra, Sulawesi, or
Borneo are interpreted as the most important source.
New Guinea is the most likely source of dispersals to
Australia, the Marquesas/ Society Islands, and the
Solomon Islands under all models.
Discussion
Phylogenetic patterns and relationships
There was no incongruence between the nuclear
and chloroplast datasets in our large Malesian sample
and hence no detectable evidence of hybridisaon. This
is in marked contrast to previous phylogenec studies
of Cyrtandra, where extensive hybridisaon and/or
incomplete lineage sorng has been reported, principally
in Hawaii (Pillon et al. 2013, Johnson et al. 2019) but
also in the recent radiaon of the genus in the Pacic
(Johnson et al. 2017). This also diers from the ecologically
and biogeographically similar genus Begonia, where
the high prevalence of hybrid events is considered to
be an important factor driving genomic change and
species evoluon (Hughes et al. 2018). A recent study
of reproducve isolaon in four species of Hawaiian
Cyrtandra showed that boundaries between sympatric
Cyrtandra species are maintained predominantly
through postzygoc barriers (Johnson et al. 2015).
In Hawaii, all 60 species are the result of a single
dispersal event to the archipelago < 5 ma (Cronk et al.
2005, Clark et al. 2008, 2009, Johnson et al. 2017), and
species are remarkably similar in oral morphology
and ecological preference, such that hybridisaon is
Atkins et al.
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Molecular phylogeny of southeast Asian Cyrtandra
Figure 4. Bayesian inference tree of Cyrtandra based on the combined ITS, psbA-trnH, rpl32‑trnL, trnL‑F, and matK regions
and highlighng the three most basal clades (A, B and C). Node support is indicated as Maximum likelihood Bootstrap
support (ML‑BS), Maximum Parsimony Bootstrap support (MP‑BS), and Bayesian Posterior Probabilies (BI‑PP). Maximum
values (100% BS or 1.0 PP) are indicated by *. No support (< 50% BS or 0.50 PP) is indicated by ‑. Species names are
colour‑coded by geographic region. Pacic islands not shown on map.
Atkins et al.
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Molecular phylogeny of southeast Asian Cyrtandra
Figure 5. Bayesian inference tree of Cyrtandra based on the combined ITS, psbA-trnH, rpl32‑trnL, trnL‑F, and matK regions,
and highlighng clades D‑J. Node support is indicated as Maximum Likelihood Bootstrap Support (ML‑BS), Maximum
Parsimony Bootstrap Support (MP‑BS), and Bayesian Posterior Probabilies (BI‑PP). Maximum values (100% BS or 1.0 PP)
are indicated by *. No support (< 50% BS or 0.50 PP) is indicated by ‑. Species names are colour‑coded by geographic
region. Pacic islands not shown on map.
Atkins et al.
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Molecular phylogeny of southeast Asian Cyrtandra
Figure 6. Maximum clade credibility tree of Cyrtandra based on a BEAST analysis of the combined ITS, psbA-trnH, rpl32‑trnL,
trnL‑F, and matK regions. Mean divergence me esmates are shown as millions of years ago (Ma), with the blue boxes
showing the 95% highest posterior density (HPD). Pliocene is abbreviated to Pli and Pleistocene to Ple in the Time Scale
below the tree.
Atkins et al.
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Molecular phylogeny of southeast Asian Cyrtandra
Figure 7. Ancestral range esmaon for Cyrtandra based on the ultrametric tree produced in BEAST, and the best model
determined by BioGeoBEARS (BayArea‑like +J). Areas are colour‑coded for the 13 geographic regions used in the analysis.
Pacic islands not shown on map. Pie graphs at each node indicate the probability of a given area (or combined areas).
Atkins et al.
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Molecular phylogeny of southeast Asian Cyrtandra
Figure 8. Summary of dispersal events in Cyrtandra esmated using a Biogeographic Stochasc Mapping (BSM) analysis in
BioGeoBEARS based on the best t model of BayArea+J (full results given in Table 6). The weight of each line indicates the
number of predicted dispersal events (both founder and range expansion). All event counts of 0.9 and above are included.
Table 6. Summary of all dispersal counts for Cyrtandra averaged across 100 BSMs in BioGeoBEARS. Mapping was performed
using parameters from the best‑t model of BayArea‑like+J. Colour temperature indicates the frequency of events,
with warmer colours indicang more common events (Red = >2.9, Orange = 2.0‑2.9, Yellow = 0.9‑1.9, Green = < 0.9).
The ancestral states (i.e., where the lineage dispersed from) are given in the row, and the descendant states (where the
lineage dispersed to) are given in the column.
TO A B C D E F G H I J K L M
TOTALS As %
FROM
Hawaii
Marquesa/SI
Japan/Taiwan
Australia
Thailand
P. Malaysia
Sumatra
Borneo
Sulawesi
New Guinea
Solomon
Java/Bal
Philippines
A Hawaii 0 0.1 0 0 0 0 0 0 0 0 0 0 0 0.1 0.3
B
Marquesas/
Society Is 1.0 0 0 0 0 0 0 0 0 0 0 0 0 1.0 2.8
C Japan/ Taiwan 0000000000000 0 0
D Australia 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
E Thailand 0 0 0 0 0 0.5 0 0 0 0 0 0 0 0.5 1.4
F Pen. Malaysia 0 0 0 0 0.5 0 0.5 0 0 0 0 0 0 1.0 2.8
G Sumatra 0 0 0 0 1.0 2.5 0 0.1 0.5 0.1 0 1.2 0 5.4 15.3
H Borneo 0 0 0 0 0.5 2.0 3.0 0 1.5 0.9 0 0.9 2.7 11.5 32.7
I Sulawesi 0 0 0 0 0 0 0.5 0 0 0 0 0 0.2 0.7 2.0
JNew Guinea 0 0.9 0 1 0 0 0 0.1 0.1 0 1 0.1 0.2 3.4 9.7
K
Solomon
Islands
0000000000000 0 0
LJava and Bali 0 0 0 0 0 0 3.0 0 1.0 0.1 0 0 0.1 4.2 11.9
MPhilippines 0 0 1.5 0 0 0 0 0.1 3.9 0.9 0 1 0 7.4 21.0
TOTALS
1 1 1.5 1 2 5 7 0.3 7 2 1 3.2 3.3 35.3
As % 2.8 2.8 4.2 2.8 5.7 14 20 0.8 20 5.7 2.8 9.1 9.3 100
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Molecular phylogeny of southeast Asian Cyrtandra
widespread. In contrast, sympatric Malesian Cyrtandra
are more likely to be from distantly related lineages
(Bramley et al. 2004a), and this is reected by the
higher level of oral divergence (Fig. 2) and apparent
lack of hybridisaon amongst sympatric species, all of
which is congruent with pre‑zygoc barriers playing a
large role in maintaining species boundaries.
The majority of the 36 named taxa that were
represented by more than one sample resolved as
monophylec with strong support, including two species
with mul‑island distribuons, C. umbellifera from
Taiwan and the northern Philippines (Clade J, Fig. 5)
and C. sandei from Java and Sumatra (Clade F, Fig. 5).
There were four cases where morphologically similar
species pairs resolve as paraphylec with respect to
each other, such as the red‑owered C. clarkei and
C. kermesina from Sabah (Clade B, Fig. 4). We might
expect to see examples such as this in a recently
evolved group where weak gene ow may be a barrier
to regaining monophyly following speciaon, as has
been recorded elsewhere in Gesneriaceae (Hughes et al.
2005). The most striking examples of polyphyly are
seen in the widespread and morphologically variable
C. pendula and C. picta, distributed across a number
of islands. Given paerns elsewhere in the genus, it
seems likely that these species names do not represent
natural groups but rather a phenec assemblage which
will need to be addressed through further collecng
and revisionary work.
Cyrtandra species in New Guinea appear to have
much wider distribuons than are typically found
elsewhere in Malesia (Atkins et al. 2019). This may
indicate a shi in dispersal ability as so many of the
New Guinea species have eshy fruits. Alternavely,
this may signal that these taxa represent very recent
radiaons that have not yet been subjected to range
contracons or exncon.
Divergence times
The origin and early diversicaon of Cyrtandra
in the region dates to the mid Miocene (crown age
13 Ma), and most of the current diversity in Southeast
Asia is the result of speciaon in the last 5 Ma (Fig. 6).
These dates are similar to those reported for Cyrtandra
in Roalson and Roberts (2016) and Johnson et al.
(2017) and signicantly younger than those reported
in Clark et al. (2008, 2009). These last, much earlier,
dates were based strictly on the geological ages of
islands, an approach which has been shown to be
problemac (Renner 2005, Heads 2011). The slightly
younger stem age recovered in the present analysis is
likely due to the inclusion of Loxosgma, an outgroup
taxon that is more closely related to Cyrtandra than
those used in earlier Cyrtandra-focused studies.
This paern of origin in the mid Miocene and
young species, mostly the result of speciaon in the
last 5 My, is reported in other Southeast Asian taxa
such as Begonia (Thomas et al. 2012) and Aglaia
(Grudinski et al. 2014), and it is highlighted by de
Bruyn et al. (2014) in their meta‑analysis of regional
biodiversity. There are a number of geological factors
which are likely to have been drivers of diversicaon
during this period. Approximately 23 Ma the Sunda and
Sahul shelves moved closer together, creang land in
the centre of the region for the rst me (Hall 2002,
2012a, b). The subsequent rapid orogenesis on key
islands such as Sulawesi and New Guinea (Hall 2002,
Hall 2012a, b) also created new habitat. Finally, the
climate and sea‑level uctuaons of the Pleistocene
resulted in cyclic vicariance with frequent habitat
fragmentaons and amalgamaons (Voris 2000,
Woodru 2010, Cannon 2012, Morley 2012).
The mean diversicaon rate for Cyrtandra in
Southeast Asia is 0.49 net speciaon events per
million years, signicantly higher than the rate of
0.089 calculated by Magallon and Sanderson (2001)
for angiosperms as a whole. The rates of Southeast
Asian Cyrtandra diversicaon are comparable to
that of the ecologically similar mega‑diverse genus
Begonia in the Neotropics (0.5) and in Asia (0.61)
(Moonlight et al. 2015). They are slightly slower than in
Pacic Cyrtandra, which has a rate of 0.68 (Roalson and
Roberts 2016), and signicantly slower than lineages
of Hawaiian Cyrtandra, in which diversicaon rates as
high as 3.5 are reported (Johnson et al. 2019). In the
case of the Pacic radiaon, Roalson and Roberts
(2016) suggested that geography may have played a
signicant role in the rapid diversicaon of taxa, with
the emergence of many island archipelagos in the last
5 Ma. Addionally, a transion to eshy fruits may
have aided long‑distance dispersal by avian frugivores
from source areas in Southeast Asia, followed by
diversicaon in newly colonised island regions.
Ancestral range estimation
The island of Borneo emerges as the most likely
ancestral area for the genus and for many of the early
diverging clades of Cyrtandra (Fig. 7). Bur (2001)
speculated that Borneo represented the ‘original
heartland’ of the genus based on its high species numbers
(c. 200) and the abundant morphological diversity seen
here, including richly developed anatomical characters
such as sclereids and tracheoids, which ‘decrease in
all direcons’ from this centre. The combinaon of
Borneo’s large area, relavely stable geological history
(Hall 2012, De Bruyn et al. 2014), and extensive areas
of rainforest, even during glacial maxima (Cannon
2012), oer a compelling explanaon for this lineage
accumulaon and in-situ diversicaon. The majority
of samples from Borneo in this analysis are from NE
Borneo. Increased sampling from elsewhere on the island,
parcularly the under‑collected areas of Kalimantan,
will help clarify whether Borneo’s important role in
the development of biogeographic paerns in the
region, is largely due to the key role of NE Borneo’s
three highest mountains as signicant rainforest refugia
(as reported for birds; Sheldon 2016) or whether it is
more generally aributable to the island as a whole.
With an esmated ancestral range on the Sunda
Shelf, Cyrtandra is another example of the increasingly
well‑documented movement of taxa from the west
to east of Southeast Asia, parcularly in rainforest
lineages (Su and Saunders 2009, Richardson et al. 2012,
Thomas et al. 2012, Grudinski et al. 2014, Crayn et al.
Atkins et al.
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Molecular phylogeny of southeast Asian Cyrtandra
2015). There are examples of dispersal in the opposite
direcon, such as in Proteaceae (Barker et al. 2007)
and Myrtaceae (Sytsma et al. 2004), but there is a
disnct asymmetry (Richardson et al. 2012, Crayn et al.
2015). The west‑to‑east dispersal appears to have
been parcularly prevalent from the mid‑Miocene
onwards as warmer and weer condions prevailed,
rainforest expanded and extant land emerged east of
Wallace’s Line (Richardson et al. 2012, Grudinski et al.
2014, Crayn et al. 2015).
The earliest example of a Sahul−Sunda long distance
dispersal in this study is within Clade E at 9.6 Ma
(7.64‑11.68 Ma, 95% HPD) from Sunda to Sahul. This
is comfortably within the me‑frame of Sahul−Sunda
disjuncon events compiled by Crayn et al. (2015).
Many of the Cyrtandra taxa east of Wallace’s Line
are characterised by eshy berries as opposed to the
predominantly dry indehiscent capsules of the Sunda
shelf taxa (Fig. 1; Bur 2001, Johnson et al. 2017). This
change in fruit morphology is possibly associated with a
transion in dispersal mode from small mammal dispersal
to bird dispersal (Gille 1967, Bur 2001). A zoochorous
dispersal mode is presented by Crayn et al. (2015) as
being the most prevalent for Sunda−Sahul dispersals,
with 90% of ancestral species possessing zoochorous
propagules, and it seems likely that the transion to
eshier berries has facilitated dispersal of Cyrtandra
across the region. As the majority of the species in
the Sahul clade (Clade E), including C. viata and C.
bungahijau from New Guinea, C. baileyi from Australia,
and C. subulibractea from the Solomon Islands, have
eshy fruits (Gille 1975, Atkins et al. 2019), it seems
likely that it is the ancestral state for this clade.
Biogeographic patterns
Borneo and the islands of the Sunda shelf
Borneo is the source of the highest number
of dispersal events for Malesian Cyrtandra, with
dispersals to the Philippines, Sulawesi, Sumatra,
Peninsular Malaysia, Java, and New Guinea
originang here (Fig. 8). This is consistent with De
Bruyn et al.’s (2014) characterisaon of the island as
an evoluonary hotspot dened not only in terms of
high species numbers and in situ diversicaon but
also subsequent emigraon. High dispersal levels
between the islands on the Sunda shelf reect the
shared geological history of these connental islands,
which would have formed connuous land during at
least some of the glacial maxima (Voris 2000, Hall
2012). At these mes there would also have been
more extensive areas of rainforest (Cannon et al.
2009, 2014, Cannon 2012), facilitang exchange and
dispersal in a wet forest genus like Cyrtandra. There
are only two samples from the Sunda shelf that fall
within the large, predominantly Wallacean, clade
(Clade J, Fig 5), and these are both from Central Java,
conrming Java’s posion as anomalous, with links
both to the Sunda shelf and Wallacea, as reported
by Van Welzen et al. (2011) in their phytogeographic
study of the region.
Philippines
The Philippines represent an important secondary
source area for Cyrtandra, as well as a stepping‑stone
for dispersal to some of the more distant regions such
as Taiwan and Japan and New Guinea (Fig. 8, Table 6).
Dispersal events from the Philippines were recovered
south to Sulawesi, north to Taiwan and southern Japan,
east to New Guinea, and even south‑west to Java.
The very dierent posion of the Philippine islands
10 Ma, when Cyrtandra was diversifying, with southern
Philippine islands such as Mindanao located much closer
to the equator (Hall 2002, Hughes et al. 2015), oers
an explanaon for the key role of the Philippines as a
route through the region. The Philippines is an area of
high species diversity for the genus, with c. 150 species
already recorded and new species sll being described
(Olivar et al. in press). Species from these islands are
morphologically very diverse and there are a number
of species with eshy fruits in the Philippines, notably
C. hirgera from Palawan and C. fragilis from Negros
and Mindanao, which is congruent with the high vagility
of lineages in the Philippine clades. For Cyrtandra,
the earliest diverging branch of Philippine taxa are
from Palawan and Camiguin (Clade G), dang to just
before 10 Ma, suggesng that the Philippines were
colonised relavely early in the diversicaon of the
genus and that both short and longer distance dispersal
from Borneo played a part in the colonisaon of the
archipelago. Our results provide some support for the
theory that Palawan, or some part of it, could have
been above sea level signicantly earlier than the start
of the Pliocene c. 5 Ma, as proposed for the Palawan
Ark Hypothesis (Blackburn et al. 2010, Siler et al.
2012). These results would also require Camiguin to
be above sea level earlier than the esmated 2 Ma
maximum age for this island (Steppan et al. 2003),
although incomplete sampling, parcularly from
nearby islands in the archipelago, could also explain
the discrepancies in dates.
Sulawesi
Sulawesi is an area of signicant immigraon,
being the recipient of 20% of all dispersals, the joint
highest in our analysis (Table 6), with dispersals
from Java, the Philippines and Borneo. In contrast,
dispersal events from Sulawesi to surrounding islands
were very infrequent (0.5 events to Sumatra and
0.2 events to the Philippines, Table 6, Fig. 8). It is
notable that although eshy fruited Cyrtandra species,
such as the unusual epiphyc C. purpurea, occur on
Sulawesi, the majority of species, and all of the most
common species, on the island, such as C. hypogaea,
C. polyneura and C. kinhoii, are characterised by the
drier, tough‑walled fruits typical of the Sunda shelf. This
low level of emigraon and the relave insignicance
of Sulawesi in terms of a dispersal route across the
region is, however, also seen in other groups such as
Begonia (Thomas et al. 2012). Sulawesi is encircled
by biogeographic boundaries, including Wallace’s and
Huxley’s line to the west, and Weber’s and Lydekker’s
to the east, suggesng that there are real barriers to
dispersal in this area. However, immigraon on to the
Atkins et al.
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Molecular phylogeny of southeast Asian Cyrtandra
island, parcularly from the Philippines and Borneo
across the western lines, has clearly occurred more
than once in Cyrtandra. Sulawesi’s highly dynamic
geological history (Hall et al. 2012a, Stelbrink et al.
2012) and the resultant increase in habitat diversity
and available niche space for colonising species, oers
a possible explanaon for the high level of immigraon
and establishment on the island. Dispersal back
across Wallace’s line from Sulawesi and successful
establishment on the Sunda shelf islands appears to
have been dicult for Cyrtandra, possibly due to niche
pre‑empon in the older, more established forests
of those islands. Increased sampling of Cyrtandra
from the islands east of Sulawesi, parcularly from
the Moluccas and New Guinea, will help illuminate
whether there is a barrier in this direcon or whether
this is an artefact of sampling.
New Guinea and the Pacic
New Guinea is resolved as the most likely source of
dispersals to Australia, the Solomon Islands, and French
Polynesia for Cyrtandra (Fig. 8, Table 6). West‑to‑east
dispersal paerns have been well documented from New
Guinea into the eastern Pacic (Keast 1996). Cyrtandra
is notable for being the only Malesian Gesneriaceae
genus with a distribuon that extends signicantly
into the Pacic (Hilliard and Bur 2002). The large
Malesian genera Aeschynanthus and Agalmyla have
wind‑dispersed seeds and, despite being highly diverse
in New Guinea, do not extend beyond the Solomon
Islands and the Louisade Archipelago (Hilliard and Bur
2002), respecvely. Johnson et al. (2017) reported
strong asymmetry in the direcon of founder events in
their study of Cyrtandra in the Pacic, with the majority
of dispersals occurring from a west‑to‑east direcon,
which they postulated to be the result of bird dispersal.
The routes to Australia and the Solomon Islands found
here were reported by Johnson et al. (2017) and were
suggested by Gille (1975) based on his extensive
knowledge of the Cyrtandra of New Guinea and the
Pacic. He reported strong morphological anies
between the Cyrtandra of New Guinea and the Bismarck
Archipelago and Solomon Islands, and an aenuaon
of morphological diversity with increasing distance
from New Guinea into the Pacic (Gille 1975). The
longest‑distance dispersal event in this study is from
New Guinea (Clade I, from Mt Jaya in the far western
part of the main cordillera) to the Marquesas/Society
Islands. However, this result is most likely an artefact
of the relavely low level of sampling from the South
Pacic in this study. In the study by Johnson et al.
(2017), which included higher density sampling of
Pacic taxa, the Marquesan lineage is the result of a
single dispersal event from Samoa, while the Society
Islands taxa are the result of two dispersal events, one
from Fiji and one from Samoa.
Conclusions
Using a robust and well sampled phylogenec tree
to study evoluonary relaonships and biogeographical
processes in Southeast Asian Cyrtandra, we found
evidence in support of (i) Borneo as the most likely
ancestral area for the genus, (ii) west‑to‑east dispersal
across the region and into the Pacic, (iii) the Philippines
as an important secondary source area and stepping
stone to Wallacea, Taiwan and Japan, and New Guinea,
and (iv) a mid‑Miocene origin for the genus with most
of the extant diversity being the result of speciaon
in the last 5 Ma. These paerns are increasingly
well‑documented and are beginning to form an emerging
paradigm for Southeast Asian plant biogeography.
The present study has provided further insight into
the fundamental quesons of when and where plant
diversicaon took place in Southeast Asia and the
role of geo‑tectonic and climac processes in shaping
the orisc composion of the area and seng the
stage for signicant species diversicaons. Further
work is needed to understand niche evoluon and
the genomic basis of adaptaon to unravel how the
massive species richness of Cyrtandra evolved and
how it is maintained.
Acknowledgements
We thank the Edinburgh Botanic Garden (Sibbald)
Trust, the Elvin McDonald Research Endowment Fund
(The Gesneriad Society), the RBGE Travel Fund, the
James & Eve Benne Trust, the Royal Horcultural
Society, and Davis Expedition Fund for funding.
The Royal Botanic Garden Edinburgh is supported
by the Rural and Environment Science and Analycal
Services Division (RESAS) of the Scosh Government.
In Indonesia, we would like to thank RISTEKDIKTI,
the Indonesian Ministry of Forestry, and sta at the
Kebun Raya Bogor, Herbarium Bogoriense, Forestry
Research Instute of Manado and Andalas University.
We parcularly thank Joeni Rahajoe, Wisnu Ardi,
Marlina Ardiyani, Hendrian, Julianus Kinho, Deden
Girmansyah, and Nurainas for assistance with permits
and collecng. In Malaysia, we would like to thank sta
at the Forest Research Instute Malaysia, parcularly
Ruth Kiew and Sam Yen Yen, the Tree Flora of Sabah and
Sarawak programme, Postar Miun, Joan Pereira, Susana
Sabran, and Julia Sang. Fieldwork in the Philippines
over many years was facilitated by the Philippine
Naonal Herbarium, Mina L. Labugen (DENR), and
Aurea L. Feliciana (Isabela State University). We would
also like to thank Masatsugu Yokota (Univ. Ruykyus,
Japan) and Ching‑I Peng (Academia Sinica, Taiwan).
Addional samples were generously provided by RBG
Kew, Shelley James (Florida Museum of Natural History,
Bishop Museum, Honolulu), Wisnu Ardi (Bogor Botanic
Garden), Deden Girmansyah (Herbarium Bogoriense),
M. Poopath (Thailand), and Michael Kiehn (Vienna
Botanic Garden); and from RBGE (in alphabecal
order) George Argent, Sadie Barber, B.L.Bur, Quenn
Cronk, Andy Ensoll, Louise Galloway, Olive Hilliard,
Mary Mendum, David Middleton, Mark Newman, Axel
Poulsen, Carmen Puglisi, Steve Sco, Daniel Thomas,
and Peter Wilkie.
We would like to thank Prof Gao Lian Ming, Kunming
Instute of Botany, Chinese Academy of Sciences,
Atkins et al.
Frontiers of Biogeography 2020, 12.1, e44814 © the authors, CC-BY 4.0 license 16
Molecular phylogeny of southeast Asian Cyrtandra
Yunnan, China, for the gi of cpDNA sequences of
two of the outgroup samples which was funded by
Grant No. 2017‑LSFGBOWS‑01 from the Large‑scale
Scienc Facilies of the Chinese Academy of Sciences.
At RBGE, we would like to thank Steve Sco, Sadie
Barber, and Nathan Kelso for excellent care of the
Cyrtandra living collecons, and Michelle Hart, Laura
Forrest, and Ruth Hollands for expert advice in the
molecular laboratories. Assistance with the programme
BioGeoBEARS was generously given by Nick Matzke.
Thanks also to Jay Edneil Olivar for enormous help
with naming of the Philippine samples included in
the analysis.
Supplementary Materials
The following materials are available as part of
the online arcle from hps://escholarship.org/uc/
Table S1. Taxon list for samples in the current study.
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Edited by Roy Erkens and Robert J. Whiaker
... The region of Tropical Southeast Asia and the Malay Archipelago (Malesia) is a very appealing area for research due to its outstanding biodiversity, being one of the most species-rich areas in the world (Lohman et al., 2011;Grudinski et al., 2014;Atkins et al., 2020), with high levels of endemism, and a complex geological history (Hall, 2002(Hall, , 2009Grudinski et al., 2014). The area harbors 20%-25% of the world's vascular plants and is the meeting point of many biota from various origins (Woodruff, 2010;Richardson et al., 2012;Zhou et al., 2019). ...
... The Malesian region, as part of Southeast Asia, extends from the Malay Peninsula eastward to Papua New Guinea (van Steenis, 1950;Raes & van Welzen, 2009) and contains an estimated 42 000 plant species, of which 70% are endemic (Roos, 1993;van Welzen et al., 2005). The high biodiversity is to a high extent the result of the very complex plate tectonic movements and resulting islands and orogenesis during the last 50 million years (Hall, 2009;Woodruff, 2010;De Bruyn et al., 2014;Atkins et al., 2020). Plant dispersals in Malesia have facilitated the floristic exchange between the continents of Asia and Australia (Crayn et al., 2015;Buerki et al., 2016;Thomas et al., 2017). ...
... Phytogeographically, Malesia can be separated into three main subregions, coinciding with three of the biodiversity hotspots: West Malesia or the Sunda Shelf, Wallacea, and east Malesia or the Sahul Shelf (New Guinea) (Raes & van Welzen, 2009;Atkins et al., 2020). All area of Malesia (except Palawan and a few neighboring islands that rafted from China) originated at some time from the Southeast Asian part of Eurasia and Australian part of Gondwana, whereby west Malesia and parts of Southeast Asia mainland, split off as various terranes, arrived much earlier at their more or less present position than the Wallacean Islands and the Sahul Shelf. ...
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The region of Tropical Southeast Asia and the Malay Archipelago is a very appealing area for research because of its outstanding biodiversity, being one of the most species‐rich areas in the world with high levels of endemism, and because of its complex geological history. The high number of species in tribe Dissochaeteae (Melastomataceae) and their tendency to narrow endemism makes the tribe an ideal group for examining biogeographic patterns. We sampled 58 accessions spread over 42 accepted and two undescribed species of the Dissochaeteae. Two nuclear (ETS, ITS) and four chloroplast regions (ndhF, psbK‐psbL, rbcL, rpl16) were used for divergence time estimation and ancestral area reconstruction. Results from the molecular dating analysis suggest that the diversity of Dissochaeteae in the Southeast Asian region resulted from a South American ancestor in the late Eocene. The ancestor of the Dissochaeteae might have migrated from South America to Southeast Asia via North America and then entered Eurasia over the North Atlantic land bridge during the Eocene. The origin and early diversification of the Dissochaeteae in Southeast Asia dates back to the middle Oligocene, and most of the genera originated during the Miocene. Indochina and Borneo are most likely the area of origin for the most recent common ancestor of the Dissochaeteae and for many of the early diverging clades of some genera within Southeast Asia. This article is protected by copyright. All rights reserved.
... The methods used here follow those detailed in Atkins et al. (2020). Total genomic DNA was extracted from fresh leaf material or silica-dried material using a modified CTAB procedure (Doyle and Doyle 1987) or using the Qiaxtractor (Qiagen, Hilden, Germany). ...
... There is a marked difference in fruit type between dry, indehiscent capsules in the west of Cyrtandra's distribution and fleshy berries in the east (Burtt 2001;Johnson et al. 2017;Atkins et al. 2020). Fleshiness is, however, Kartonegoro et al. (2018) challenging to score for Cyrtandra. ...
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Cyrtandra (Gesneriaceae), with over 800 species, is a mega-diverse genus which presents considerable taxonomic challenges due to its size. A well-sampled phylogeny of the genus across Southeast Asia has confirmed that all but one of the sections within Clarke’s 1883 genus-wide infrageneric classification are polyphyletic. It also shows that there are high levels of homoplasy in key morphological characters, although it is possible to use morphological characters to define clades in parts of the phylogenetic tree. There is some geographic structure in the phylogeny, but there is also evidence of dispersal between islands. A practical approach for tackling the taxonomy of Cyrtandra in the region, through phylogenetically informed taxonomic revisions of geographic areas, an approach which combines evidence from molecular, morphological and distribution data, is discussed. Completing our understanding of species diversity and delimitation in this genus will allow us to maximise the use of Cyrtandra as a tool for studying biogeography, speciation, diversification and conservation prioritisation in the rainforests of Southeast Asia.
... The existence of a large area of suitable habitat into which propagules could disperse makes long distance dispersal more likely to occur. In fact, the large area and relative geological stability of Borneo, coupled with the persistence there of large tracts of rainforest during Pleistocene glacial maxima might have made it a cradle of diversification (de Bruyn et al., 201 Hall, 2012Lohman et al., 2011, e.g. in the exceptionally diverse genus Cyrtandra ( esneriaceae) (Atkins et al., 2020). Either way, after the divergence of O. trinervis C (O. trinervis W3 0), the remainder of this clade became O. rubescens, which spread via at least seven dispersal events across the entire region, including a back-dispersal to mainland SE Asia via Sumatra (Fig. ). ...
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Climate change and geological events have long been known to shape biodiversity, implying that these can likewise be viewed from a biological perspective. To study whether plants can shed light on this, and how they responded to climate change there, we examined Oreocnide, a genus widely distributed in SE Asia. Based on broad geographic sampling with genomic data, we employed an integrative approach of phylogenomics, molecular dating, historical biogeography, and ecological analyses. We found that Oreocnide originated in mainland East Asia and began to diversify ∼6.06 Ma, probably in response to a distinct geographic and climatic transition in East Asia at around that time, implying that the last important geological change in mainland SE Asia might be 1 Ma older than previously suggested. Around four immigration events to the islands of Malesia followed, indicating that immigration from the mainland could be an underestimated factor in the assembly of biotic communities in the region. Two detected increases of diversification rate occurred 3.13 and 1.19 Ma, which strongly implicated climatic rather than geological changes as likely drivers of diversification, with candidates being the Pliocene intensification of the East Asian monsoons, and Pleistocene climate and sea level fluctuations. Distribution modelling indicated that Pleistocene sea level and climate fluctuations were inferred to enable inter-island dispersal followed by allopatric separation, underpinning radiation in the genus. Overall, our study, based on multiple lines of evidence, linked plant diversification to the most recent climatic and geological events in SE Asia. We highlight the importance of immigration in the assembly and diversification of the SE Asian flora, and underscore the utility of plant clades, as independent lines of evidence, for reconstructing recent climatic and geological events in the SE Asian region.
... Within the Indo-Malayan Realm, recent phylogenetic studies across several angiosperm families have shown that geoclimatic events such as monsoon intensification (Sen et al., 2019;Ding et al., 2020;Surveswaran et al., 2020), aridification (Klaus et al., 2016), mountain orogeny (Meng et al., 2015;Zhao et al., 2016;Shrestha et al., 2018;Yang et al., 2018;Ding et al., 2020), Pleistocene glaciation (Ding et al., 2020), and Pleistocene sea-level changes (Givnish et al., 2016;Atkins et al., 2020) have played major roles in driving lineage diversifications. The time period of these lineage diversifications has been identified to be recent, often ranging from c.15 to 4 Ma (Manish and Pandit, 2018). ...
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The Indo-Malayan Realm is a biogeographic realm that extends from the Indian Subcontinent to the islands of Southeast Asia (Malay Archipelago). Despite being megadiverse, evolutionary hypotheses explaining taxonomic diversity in this region have been rare. Here, we investigate the role of geoclimatic events such as Himalayan orogeny and monsoon intensification in the diversification of the ginger lilies (Hedychium J.Koenig: Zingiberaceae). We first built a comprehensive, time-calibrated phylogeny of Hedychium with 75% taxonomic and geographic sampling. We found that Hedychium is a very young lineage that originated in Northern Indo-Burma, in the Late Miocene (c. 10.6 Ma). This was followed by a late Neogene and early Quaternary diversification, with multiple dispersal events to Southern Indo-Burma, Himalayas, Peninsular India, and the Malay Archipelago. The most speciose clade IV i.e., the predominantly Indo-Burmese clade also showed a higher diversification rate, suggesting its recent rapid radiation. Our divergence dating and GeoHiSSE results demonstrate that the diversification of Hedychium was shaped by both the intensifications in the Himalayan uplift as well as the Asian monsoon. Ancestral state reconstructions identified the occurrence of vegetative dormancy in both clades I and II, whereas the strictly epiphytic growth behavior, island dwarfism, lack of dormancy, and a distinct environmental niche was observed only in the predominantly island clade i.e., clade III. Finally, we show that the occurrence of epiphytism in clade III corresponds with submergence due to sea-level changes, suggesting it to be an adaptive trait. Our study highlights the role of recent geoclimatic events and environmental factors in the diversification of plants within the Indo-Malayan Realm and the need for collaborative work to understand biogeographic patterns within this understudied region. This study opens new perspectives for future biogeographic studies in this region and provides a framework to explain the taxonomic hyperdiversity of the Indo-Malayan Realm.
... Additional data were downloaded from the Global Biodiversity Facility (http:// www.gbif.org). Atkins et al. (2020) noted that the sampling density can also impact the historical biogeography analyses, thus a comparison of our sampling rates against current species estimates to evaluate the impact of sampling density on the results is presented in Tab. S2. ...
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Alpinia Roxb. is considered the largest genus of Zingiberaceae with ca. 250 species occurring in tropical and subtropical Asia, Australia, and Pacific Islands. The historical biogeography of Alpinia was conducted to explain where Alpinia originated and how it migrated to other regions. The phylogeny, divergence times and ancestral area reconstruction of Alpinia were performed by using the molecular data based on the comprehensive taxon sampling. Our results provide an objective approach to understand the historical biogeography of Alpinia. The genus originated in Asia during the Late Cretaceous ca. 69 Ma and started to diverge after the K–Pg boundary during the early Paleocene with the presence and development of the tropical rainforest and a warm, moist climate. Alpinia migrated to Malesia and then dispersed to Australasia. The molecular analyses supported the diversification of Alpinia in Asia and Malesia. Additionally, the Indian Alpinia has likely a common ancestor with Renealmia and Aframomum, and it is possible that after originating in Asia, Alpinia migrated from Asia to India then to Africa during the early period of collision between the Indian subcontinent and Eurasia to form the common ancestor of Indian Alpinia, Renealmia, and Aframomum. Our phylogeny provides a framework for studies in biogeography, comparative ecology, and evolution.
... The genus has evidently spread from Borneo to other areas, including independent range extensions to Thailand and Peninsular Malaysia, within the last c. 4-10 million years (Atkins et al., 2020). A similar pattern has been observed in Alocasia (Nauheimer et al., 2012) and Musa Colla (Janssens et al., 2016). ...
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... The analyses of these sequence data using supermatrix approaches also provided large scale phylogenetic hypotheses for the entire family (768 species; Roalson and Roberts, 2016) and the Gesnerioideae subfamily (583 species; Serrano-Serrano et al., 2017). However, the limited number of informative sites provided by these DNA regions currently hinders our understanding of the phylogenetic relationships within the most diverse genera such as Besleria (Clark et al., 2006), Columnea (Schulte et al., 2014), Cyrtandra (Atkins et al., 2019), and Streptocarpus (Nishii et al., 2015). In addition, the few available nuclear sequences (e.g. ...
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In this chapter we attempt to determine the contribution of Sundanian elements to Australasian land masses and vice versa, and to offer explanations for any bias in the direction of dispersal. We refer to the origin of a group as being Sundanian or Australasian (i.e. to the west or east of Wallace’s Line , respectively) rather than Gondwanan or Laurasian. This is because some Sundanian elements may have had a Gondwanan origin, having arrived in Sundania via the former Gondwanan land mass of India. Our focus will be on the interchange of everwet forest elements and to a lesser extent the montane vegetation. We summarise current vegetation patterns and discuss traditional approaches to assessing biotic interchange based on floristic composition and fossils. We assess the contribution of dated molecular phylogenetic trees to describe these patterns, reassess overall plant dispersal patterns in the Malesian region, and discuss which variables may be important in controlling successful colonisation.
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Eleven new species of Cyrtandra (Gesneriaceae) from Sulawesi are described and illustrated: C. albiflora Karton. & H.J.Atkins, C. boliohutensis Karton. & H.J.Atkins, C. gambutensis Karton. & H.J.Atkins, C. hekensis Karton. & H.J.Atkins, C. hendrianii Karton. & H.J.Atkins, C. hispidula Karton. & H.J.Atkins, C. kinhoii Karton. & H.J.Atkins, C. multinervis Karton. & R.Bone, C. nitida Karton. & H.J.Atkins, C. rantemarioensis Karton. & R.Bone and C. rubribracteata Karton. & H.J.Atkins. Illustrations, maps and preliminary conservation assessments are provided for all the species.
Thesis
The plant family Gesneriaceae is represented in Sri Lanka by six genera: Aeschynanthus, Epithema, Championia, Henckelia, Rhynchoglossum and Rhynchotechum, with 13 species (plus one subspecies/variety) of which ten are endemic including the monotypic genus Championia, according to the last revision in 1981. They are exclusively distributed in undisturbed habitats, and some have high ornamental value. The species are morphologically diverse, but face a problem of taxonomic delineation, which is further complicated by the presence of putative hybrids. Sri Lanka and Indian Peninsula, represent the Deccan plate of the ancient Gondwanan supercontinent. The presence of a relict flora may indicate the significance of the geological history of the Deccan plate for the evolution of angiosperms. The high degree of endemism here, along with their affinities to the global angiosperm flora paints a complex picture, but its biogeographic history is still unclear. The pantropical family Gesneriaceae distributed in Sri Lanka and South India is therefore an appropriate study group in this context. Besides, the family itself has a complex but largely unresolved biogeographical history especially concerning the origin and diversification of Old World Gesneriaceae. Modern approaches for the taxonomic studies were applied, integrating morphological and molecular data. Multiple samples were collected for each species across their geographical distribution. Nuclear ITS and chloroplast trnL-F sequences for the taxa from Sri Lanka were used to generate regional genus phylogenies of all six genera, using maximum parsimony. The rate of evolution of the nuclear ITS region versus chloroplast trnL-F was varied greatly across the six genera studied. Molecular delimitations were mostly congruent with the classical taxonomy. Over 65 taxonomic characters were studied in detail to recognize synapomorphies for clades and taxa. A complete taxonomic revision of Gesneriaceae in Sri Lanka, including lectotypification, was conducted based on both, the molecular and morphological data. This resulted in the recognition of 14 species in the six genera, including one newly described species H. wijesundarae Ranasinghe and Mich.Möller. Henckelia communis and H. angusta were not supported molecularly as two separate entities but are recognized as two species because of consistent morphological differences between them. Henckelia humboldtiana is proposed to represent a species complex due to its highly variable and inconsistent molecular and morphological diversity and overlap with H. incana and H. floccosa; more research is needed here. National conservation assessments were conducted, and all 14 species were recognized as threatened. Biogeographic affinities of Sri Lankan Gesneriaceae were elucidated, generating a dated phylogeny using an existing matrix of four plastid gene regions; trnL-F, matK, rps16 and ndhF, amended by sequences generated in this study. The final combined matrix included 175 taxa including newly generated sequences for the 13 Sri Lankan taxa. Phylogenetic trees were generated using parsimony, maximum likelihood and Bayesian inference. Molecular dating was carried out using BEAST and ancestral area reconstruction using BioGeoBears. These analyses indicated that the six genera of Gesneriaceae arrived in Sri Lanka separately and sometimes different time periods. One lineage dated back to the early diversification of the subfamily Didymocarpoideae (generally regarded as the Old World Gesneriaceae), which occurred around the KT boundary, before the Deccan plate was connected to Asia.